Challenges for identifying the neural mechanisms that support spatial navigation: the impact of spatial scale

Abstract

Spatial navigation is a fascinating behavior that is essential for our everyday lives. It involves nearly all sensory systems, it requires numerous parallel computations, and it engages multiple memory systems. One of the key problems in this field pertains to the question of reference frames: spatial information such as direction or distance can be coded egocentrically-relative to an observer-or allocentrically-in a reference frame independent of the observer. While many studies have associated striatal and parietal circuits with egocentric coding and entorhinal/hippocampal circuits with allocentric coding, this strict dissociation is not in line with a growing body of experimental data. In this review, we discuss some of the problems that can arise when studying the neural mechanisms that are presumed to support different spatial reference frames. We argue that the scale of space in which a navigation task takes place plays a crucial role in determining the processes that are being recruited. This has important implications, particularly for the inferences that can be made from animal studies in small scale space about the neural mechanisms supporting human spatial navigation in large (environmental) spaces. Furthermore, we argue that many of the commonly used tasks to study spatial navigation and the underlying neuronal mechanisms involve different types of reference frames, which can complicate the interpretation of neurophysiological data.

Keywords: allocentric and egocentric representation; environmental space; hippocampus; reference frames; spatial navigation; vista space.

Figure 1

Egocentric and allocentric relationships.

Figure 2

Vista spaces: the yellow polygon despicts the area of St Peters square that is visible from the observer position (x). Note that almost the entire space can be apprehended from a single position. While visual barrieres such as the obelisk and the fountains will obstruct the view of some of the space, only little exploratory movements are required to apprehend the entire space. The visible area from any position is crucial for defining the local vista spaces as well as connections between them (see Franz and Wiener, 2008).

Figure 3

Hierarchical graph-like representation of an environmental scale space. Single places or vista scale spaces are represented as nodes, connections between them are represented by edges. Graphs also allow to represent hierarchical spatial knowledge, where several places are combined to form regions. The spatial relationship between different regions is represented at a higher level of abstraction (Wiener and Mallot, 2003).

Figure 4

Spatial Coding in the Morris Water Maze; left: the animal has found the platform and can encode the spatial relationship between the platform and extra-maze cues as allocentric vectors. Note that while sitting on the platform, allocentric and egocentric vectors to the landmarks only differ with respect to their orientation, but not in their length; right: as the entire environment can be perceived from any position in the pool, the platform location can be computed by simply projecting the learned allocentric vectors from the landmarks into the pool. As a consequence, the animal does not need to know its current allocentric position to find the submerged platform.