Nostalgia enhances route learning in a virtual environment.

Salient landmarks enhance route learning. We hypothesised that semantically salient nostalgic landmarks would improve route learning compared to non-nostalgic landmarks. In two experiments, participants learned a route through a computer-generated maze using directional arrows and wall-mounted pictures. On the test trial, the arrows were removed, and participants completed the maze using only the pictures. In the nostalgia condition, pictures were of popular music artists and TV characters from 5 to 10 years ago. In the control condition, they were recent pictures of these same artists and characters. In Experiment 1, in the test trial, participants in the nostalgia condition completed the maze faster than controls. Experiment 2 conceptually replicated these findings and extended them by exploring boundary conditions. Participants had to learn two mazes sequentially. In Maze 1, we placed nostalgic/control landmarks only at non-decision points (whereas we placed them at decision points in Experiment 1). In Maze 2, we placed nostalgic/control landmarks at decision points during acquisition but removed them in the test trial (whereas they were present in the test trial in Experiment 1). In both mazes, participants in the nostalgia (compared to control) condition completed the test trial faster.

Induction of spatial anxiety in a virtual navigation environment.

Spatial anxiety (i.e., feelings of apprehension and fear about navigating everyday environments) can adversely impact people's ability to reach desired locations and explore unfamiliar places. Prior research has either assessed spatial anxiety as an individual-difference variable or measured it as an outcome, but there are currently no experimental inductions to investigate its causal effects. To address this lacuna, we developed a novel protocol for inducing spatial anxiety within a virtual environment. Participants first learnt a route using directional arrows. Next, we removed the directional arrows and randomly assigned participants to navigate either the same route (n = 22; control condition) or a variation of this route in which we surreptitiously introduced unfamiliar paths and landmarks (n = 22; spatial-anxiety condition). The manipulation successfully induced transient (i.e., state-level) spatial anxiety and task stress but did not significantly reduce task enjoyment. Our findings lay the foundation for an experimental paradigm that will facilitate future work on the causal effects of spatial anxiety in navigational contexts. The experimental task is freely available via the Open Science Framework ( https://osf.io/uq4v7/ ).

The Free-movement pattern Y-maze: A cross-species measure of working memory and executive function.

Numerous neurodegenerative and psychiatric disorders are associated with deficits in executive functions such as working memory and cognitive flexibility. Progress in developing effective treatments for disorders may benefit from targeting these cognitive impairments, the success of which is predicated on the development of animal models with validated behavioural assays. Zebrafish offer a promising model for studying complex brain disorders, but tasks assessing executive function are lacking. The Free-movement pattern (FMP) Y-maze combines aspects of the common Y-maze assay, which exploits the inherent motivation of an organism to explore an unknown environment, with analysis based on a series of sequential two-choice discriminations. We validate the task as a measure of working memory and executive function by comparing task performance parameters in adult zebrafish treated with a range of glutamatergic, cholinergic and dopaminergic drugs known to impair working memory and cognitive flexibility. We demonstrate the cross-species validity of the task by assessing performance parameters in adapted versions of the task for mice and Drosophila, and finally a virtual version in humans, and identify remarkable commonalities between vertebrate species' navigation of the maze. Together, our results demonstrate that the FMP Y-maze is a sensitive assay for assessing working memory and cognitive flexibility across species from invertebrates to humans, providing a simple and widely applicable behavioural assay with exceptional translational relevance.

Overshadowing of geometric cues by a beacon in a spatial navigation task.

In three experiments, we examined whether overshadowing of geometric cues by a discrete landmark (beacon) is due to the relative saliences of the cues. Using a virtual water maze task, human participants were required to locate a platform marked by a beacon in a distinctively shaped pool. In Experiment 1, the beacon overshadowed geometric cues in a trapezium, but not in an isosceles triangle. The longer escape latencies during acquisition in the trapezium control group with no beacon suggest that the geometric cues in the trapezium were less salient than those in the triangle. In Experiment 2, we evaluated whether generalization decrement, caused by the removal of the beacon at test, could account for overshadowing. An additional beacon was placed in an alternative corner. For the control groups, the beacons were identical; for the overshadow groups, they were visually unique. Overshadowing was again found in the trapezium. In Experiment 3, we tested whether the absence of overshadowing in the triangle was due to the geometric cues being more salient than the beacon. Following training, the beacon was relocated to a different corner. Participants approached the beacon rather than the trained platform corner, suggesting that the beacon was more salient. These results suggest that associative processes do not fully explain cue competition in the spatial domain.

Selective temporal resections and spatial memory impairment: cue dependent lateralization effects.

Patients who had undergone a unilateral trans-sylvian selective amygdalohippocampectomy as treatment for chronic intractable epilepsy were tested in a virtual Morris Water Maze (MWM) task where they were required to locate a hidden platform as a measure of spatial learning. These individuals' performance on spatial tasks was compared to age-matched healthy controls and drug-matched healthy controls. Training occurred in two different maze environments, one with conventional cues such as windows and doors, and another with abstract cues, such as colours and patterns. Participants searched for a hidden platform in the virtual pool, guided by either the conventional or abstract cues. There was a significant impairment in the surgery group compared to the control groups in all environments, however in the abstract environment only the patients with right-sided lesions were significantly worse than the controls. There was no difference between the groups on a control egocentric navigation task. These results suggest that people who have had right-sided surgery are impaired in spatial tasks, and that the level of impairment on the spatial task may be dependent on the characteristics of the cues such as how easily the cues are verbalised. These results support the notion of the functional lateralization of specific elements of spatial memory and functional lateralization, and may shed light on previous inconsistencies in this area of research.

Evidence for a shift from place navigation to directional responding in one variant of the Morris water task.

Previous work from our laboratory has demonstrated that rats display a preference for directional responding over place navigation in a wide range of procedural variants of the Morris water task (Hamilton, Akers, Weisend, & Sutherland, 2007; Hamilton et al., 2008). A preference for place navigation has only been observed when the pool is reduced as a cue by filling it with water. Studies using dry land mazes have suggested that rats place navigate early in training and later switch to other forms of responding (e.g., motor). The present study evaluated whether rats switch from place navigation to directional responding in the "full-pool" variant of the water task. Rats were given 12, 24, or 36 hidden platform training trials. Probe trials with the pool repositioned in the room revealed a preference for place navigation in rats given 12 trials, an equal division of response preferences in rats given 24 trials, and a preference for directional responding in rats given 36 trials. These results indicate that the early preference for place navigation in the full-pool water task is transient and yields to a preference for directional responding with continued training.

Control of rodent and human spatial navigation by room and apparatus cues.

A growing body of literature indicates that rats prefer to navigate in the direction of a goal in the environment (directional responding) rather than to the precise location of the goal (place navigation). This paper provides a brief review of this literature with an emphasis on recent findings in the Morris water task. Four experiments designed to extend this work to humans in a computerized, virtual Morris water task are also described. Special emphasis is devoted to how directional responding and place navigation are influenced by room and apparatus cues, and how these cues control distinct components of navigation to a goal. Experiments 1 and 2 demonstrate that humans, like rats, perform directional responses when cues from the apparatus are present, while Experiment 3 demonstrates that place navigation predominates when apparatus cues are eliminated. In Experiment 4, an eyetracking system measured gaze location in the virtual environment dynamically as participants navigated from a start point to the goal. Participants primarily looked at room cues during the early segment of each trial, but primarily focused on the apparatus as the trial progressed, suggesting distinct, sequential stimulus functions. Implications for computational modeling of navigation in the Morris water task and related tasks are discussed.

Differential place and response learning in horses displaying an oral stereotypy.

Significant similarities exist between the neural and behavioural features of environmentally and drug-induced stereotypy. For example, exposure to dopamine agonists, such as amphetamine, induces stereotypy and causes alterations in midbrain neurophysiology similar to those observed following chronic stress. An additional behavioural feature of these neural changes in the drug-induced phenotype is an enhanced rate of switching from response-outcome (R-O) to stimulus-response (S-R) learning. The aim of the current experiment was to examine R-O and S-R learning in horses displaying environmentally induced oral stereotypies. This was achieved by employing variations of the place/response paradigm. In Experiment 1, we found that crib-biting horses displayed 'response' learning after 20 learning trials, whereas non-crib-biting controls tended to display 'place' learning throughout the experiment. In Experiment 2, we used a modified version of the procedure, in which the subjects were introduced to the maze from different start points and forced always to turn the same way. We found that the crib-biters acquired the task at a faster rate suggesting again that this group was displaying 'response' learning. Finally, in Experiment 3, we carried out an arena test to ensure that crib-biters were capable of 'place' learning. These results are the first to show that horses displaying an oral stereotypy, a behavioural phenotype previously associated with stress-induced perturbations of the basal ganglia, preferentially use 'response' learning. The findings are discussed in relation to the search for an aetiological model of stereotypy.

Impaired instrumental choice in crib-biting horses (Equus caballus).

Horses displaying an oral stereotypy were tested on an instrumental choice paradigm to examine differences in learning from non-stereotypic counterparts. Stereotypic horses are known to have dysfunction of the dorsomedial striatum, and lesion studies have shown that this region may mediate response-outcome learning. The paradigm was specifically applied in order to examine learning that requires maintenance of response-outcome judgements. The non-stereotypic horses learned, over three sessions, to choose a more immediate reinforcer, whereas the stereotypic horses failed to do so. This suggests an initial behavioural correlate for dorsomedial striatum dysregulation in the stereotypy phenotype.

The relative influence of place and direction in the Morris water task.

Previous work from our laboratory has demonstrated that rats display a preference for directional responding over true place navigation in the Morris water task. The present study evaluated the range of situations in which this preference is observed and attempted to identify methods that favor navigation to the precise location of the escape platform in the room. A preference for directional responding over place navigation was observed in a wide range of procedures that included providing extensive training (Experiment 1), providing only platform placement experience in the absence of active swim training (Experiment 2), training navigation to multiple platform locations in a moving platform variant of the task (Experiment 3), and explicitly training navigation to a precise location in the room, versus navigation in a particular direction, regardless of the pool's position in the room (Experiments 4-5). A modest preference for navigation to the precise spatial location of the platform was observed when the pool wall was virtually eliminated as a source of control by filling it to the top with water (Experiment 6).

Spatial exploration patterns determine navigation efficiency: trade-off between memory demands and distance travelled.

A total of 41 participants explored a novel square-shaped environment containing five identical boxes each hiding a visually distinct object. After an initial free exploration the participants were required to locate the objects first in a predetermined and subsequently in an optional order task. Two distinct exploration strategies emerged: Participants explored either along the main axes of the room (axial), or in a more spatially spread, circular pattern around the edges of the room (circular). These initial exploration strategies influenced the optimality of spatial navigation performance in the subsequent optional order task. The results reflect a trade-off between memory demands and distance efficiency. The more sequential axial strategy resulted in fewer demands on spatial memory but required more distance to be travelled. The circular strategy was more demanding on memory but required less subsequent travelling distance. The findings are discussed in terms of spatial knowledge acquisition and optimality of strategy representations.

Multimodal discrimination learning in humans: evidence for configural theory.

Human contingency learning was used to compare the predictions of configural and elemental theories. In three experiments, participants were required to learn which indicators were associated with an increase in core temperature of a fictitious nuclear plant. Experiments 1 and 2 investigated the rate at which a triple-element stimulus (ABC) could be discriminated from either single-element stimuli (A, B, and C) or double-element stimuli (AB, BC, and AC). Experiment 1 used visual stimuli, whilst Experiment 2 used visual, auditory, and tactile stimuli. In both experiments the participants took longer to discriminate the triple-element stimulus from the more similar double-element stimuli than from the less similar single-element stimuli. Experiment 3 tested for summation with stimuli from either a single or multiple modalities, and summation was found only in the latter case. Thus, the pattern of results seen in Experiments 1 and 2 was not dependent on whether the stimuli were single modal or multimodal, nor was it dependent on whether the stimuli could elicit summation. This pattern of results is consistent with predictions derived from Pearce's (1987, 1994) configural theory.

Summation in autoshaping is affected by the similarity of the visual stimuli to the stimulation they replace.

Pigeons received autoshaping with 2 stimuli, A and B, presented in adjacent regions on a television screen. Conditioning with each stimulus was therefore accompanied by stimulation that was displaced from the screen whenever the other stimulus was presented. Test trials with AB revealed stronger responding if this displaced stimulation was similar to, rather than different from, A and B. For a further experiment the training just described included trials with A and B accompanied by an additional, similar, stimulus. Responding during test trials with AB was stronger if the additional trials signaled the presence rather than the absence of food. The results are explained with a configural theory of conditioning.