Daniele Nardi

Hippocampal size predicts rapid learning of a cognitive map in humans.

The idea that humans use flexible map‐like representations of their environment to guide spatial navigation has a long and controversial history. One reason for this enduring controversy might be that individuals vary considerably in their ability to form and utilize cognitive maps. Here we investigate the behavioral and neuroanatomical signatures of these individual differences. Participants learned an unfamiliar campus environment over a period of three weeks. In their first visit, they learned the position of different buildings along two routes in separate areas of the campus. During the following weeks, they learned these routes for a second and third time, along with two paths that connected both areas of the campus. Behavioral assessments after each learning session indicated that subjects formed a coherent representation of the spatial structure of the entire campus after learning a single connecting path. Volumetric analyses of structural MRI data and voxel‐based morphometry (VBM) indicated that the size of the right posterior hippocampus predicted the ability to use this spatial knowledge to make inferences about the relative positions of different buildings on the campus. An inverse relationship between gray matter volume and performance was observed in the caudate. These results suggest that (i) humans can rapidly acquire cognitive maps of large‐scale environments and (ii) individual differences in hippocampal anatomy may provide the neuroanatomical substrate for individual differences in the ability to learn and flexibly use these cognitive maps.

The world is not flat: Can people reorient using slope?

Studies of spatial representation generally focus on flat environments and visual input. However, the world is not flat, and slopes are part of most natural environments. In a series of 4 experiments, we examined whether humans can use a slope as a source of allocentric, directional information for reorientation. A target was hidden in a corner of a square, featureless enclosure tilted at a 5° angle. Finding it required using the vestibular, kinesthetic, and visual cues associated with the slope gradient. In Experiment 1, the overall sample performed above chance, showing that slope is sufficient for reorientation in a real environment. However, a sex difference emerged; men outperformed women by 1.4 SDs because they were more likely to use a slope-based strategy. In Experiment 2, attention was drawn to the slope, and participants were prompted to rely on it to solve the task; however, men still outperformed women, indicating a greater ability to use slope. In Experiment 3, we excluded the possibility that womens disadvantage was due to wearing heeled footwear. In Experiment 4, women required more time than men to identify the uphill direction of the slope gradient; this suggests that, in a bottom-up fashion, a perceptual or attentional difficulty underlies womens disadvantage in the ability to use slope and their decreased reliance on this cue. Overall, a bi-coordinate representation was used to find the goal: The target was encoded primarily with respect to the vertical axis and secondarily with respect to the orthogonal axis of the slope.

Slope-Driven Goal Location Behavior in Pigeons

A basic tenet of principles of associative learning applicable to models of spatial learning is that a cue should be assigned greater weight if it is a better predictor of the goal location. Pigeons were trained to locate a goal in an acute corner of an isosceles trapezoid arena, presented on a slanted floor with 3 (Experiment 1) or 2 (Experiment 2) orientations. The goal could be consistently determined by the geometric shape of the arena; however, its position with respect to the slope gradient varied, such that slope position was not a good predictor of the goal. Pigeons learned to solve the task, and testing on a flat surface revealed successful encoding of the goal relative to the geometric shape of the arena. However, when tested in the arena placed in a novel orientation on the slope, pigeons surprisingly made systematic errors to the other acute-but geometrically incorrect-mirror image corner. The results indicate that, for each arena orientation, pigeons encoded the goal location with respect to the slope. Then, in the novel orientation, they chose the corner that matched the goals position on the slope plus local cue (corner angle). Although geometry was 2 times (Experiment 2) or even 3 times (Experiment 1) as predictive as slope, it failed to control behavior during novel test trials. Instead, searching was driven by the less predictive slope cues. The reliance on slope and the unresponsiveness to geometry are explained by the greater salience of slope despite its lower predictive value.

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.

Slope-based encoding of a goal location is unaffected by hippocampal lesions in homing pigeons (Columba livia)

Using the same procedures as Nardi and Bingman (2009) [22], bilateral hippocampal lesions were found to have no detectable effect on the capacity of homing pigeons to use the slope of an inclined surface to encode a goal location. Hippocampal lesioned pigeons, like controls, also preferentially relied on slope over geometry when the two sources of information were set in conflict. As such, slope resembles visual features as a source of goal recognition information that is hippocampal independent.

Up by upwest: Is slope like north?

Terrain slope can be used to encode the location of a goal. However, this directional information may be encoded using a conceptual north (i.e., invariantly with respect to the environment), or in an observer-relative fashion (i.e., varying depending on the direction one faces when learning the goal). This study examines which representation is used, whether the sensory modality in which slope is encoded (visual, kinaesthetic, or both) influences representations, and whether use of slope varies for men and women. In a square room, with a sloped floor explicitly pointed out as the only useful cue, participants encoded the corner in which a goal was hidden. Without direct sensory access to slope cues, participants used a dial to point to the goal. For each trial, the goal was hidden uphill or downhill, and the participants were informed whether they faced uphill or downhill when pointing. In support of observer-relative representations, participants pointed more accurately and quickly when facing concordantly with the hiding position. There was no effect of sensory modality, providing support for functional equivalence. Sex did not interact with the findings on modality or reference frame, but spatial measures correlated with success on the slope task differently for each sex.

Reorientation by slope cues in humans.

Animals are remarkably skilled in their capacity to use a range of environmental features to orient in space once they have lost track of where they are, a process called reorientation. Among the types of cues that animals can use, one that has received little attention is the information extractable from a terrain extending in the vertical dimension, such as a geographical slant or slope (Miniaci et al. 1999; Proffitt et al. 1995; Restat et al. 2004). A slope gradient is a source of directional information (Jacobs and Schenk 2003), enabling a navigator to establish an allocentric reference frame based on the vertical axis (up– down) and the derived orthogonal axis (left–right) of the slope (Restat et al. 2004). The use of slope for reorientation and goal location has been shown in non-human animals (rats: Miniaci et al. 1999; pigeons: Nardi and Bingman 2009). The present research aimed to study, for the first time, if humans can reorient by a geographical slant in a real-world environment. This is an ecologically relevant question because terrain slope is part of the lay of the land in natural environments. Furthermore, although it is a perceptually salient cue, as it provides potentially redundant, multimodal sensory activations (visual, proprioceptive, kinesthetic and vestibular stimuli), hill slants tend to be misjudged, and the conscious awareness of slope seems to be highly variable, depending, for example, on physiological and psychosocial resources (Proffitt et al. 1995; Schnall et al. 2008). Method

Making a stronger case for comparative research to investigate the behavioral and neurological bases of three-dimensional navigation

The rich diversity of avian natural history provides exciting possibilities for comparative research aimed at understanding three-dimensional navigation. We propose some hypotheses relating differences in natural history to potential behavioral and neurological adaptations possessed by contrasting bird species. This comparative approach may offer unique insights into some of the important questions raised by Jeffery et al.

The role of slope in human reorientation

Studies of spatial representation generally focus on flat environments and visual stimuli. However, the world is not flat, and slopes are part of many natural environments. In a series of four experiments, we examined whether humans can use a slope as a source of allocentric, directional information for reorientation. A target was hidden in a corner of a square, featureless enclosure tilted at a 5° angle. Finding it required using the vestibular, kinesthetic and visual cues associated with the slope gradient. Participants succeeded in the task; however, a large sex difference emerged. Men showed a greater ability in using slope and a greater preference for relying on slope as a searching strategy. The female disadvantage was not due to wearing heeled shoes, but was probably related to a greater difficulty in extracting the vertical axis of the slope.

Does terrain slope really dominate goal searching

If you can locate a target by using one reliable source of information, why would you use an unreliable one? A similar question has been faced in a recent study on homing pigeons, in which, despite the presence of better predictors of the goal location, the slope of the floor in an arena dominated the searching process. This piece of evidence seems to contradict straightforward accounts of associative learning, according to which behavior should be controlled by the stimulus that best predicts the reward, and has fueled interest toward one question that, to date, has received scarce attention in the field of spatial cognition: how are vertical spaces represented? The purpose of this communication is to briefly review the studies on this issue, trying to determine whether slope is a special cue—driving behavior irrespective of other cues—or simply a very salient one.