Emergence of the Hippocampus as a Vector for Goal-Directed Spatial Navigation

The hippocampus, which is deeply involved in episodic memory, plays a pivotal role in spatial navigation, an essential animal behavior. Spatial navigation requires the calculation of the distance and direction from a current to the final position, i.e., a vector to a goal. Place cells in the mammalian hippocampus maximally increase their firing rates when the animal passes a particular location and then encode the animal's current location. The entorhinal cortex, one synapse upstream of the hippocampus, contains both grid and head direction cells that encode distance and direction information, respectively. However, the question of whether the hippocampus generates a vector for goal-directed navigation during the integration of distance and direction to the destination remains unclear. Mounting evidence of the cell types involved in spatial navigation has been obtained mainly in mammalian model animals such as rats and mice. Recent advances in wireless and miniaturized neural activity monitoring devices have begun to yield results not only in model organisms but also in wild mammals, birds, fish, and insects. A scrutiny of the literature examining neural correlates of spatial navigation across multiple animal species reveals that few place cells or grid cells have been found, but that head direction cells are commonly present in multiple animal species. Exceptionally, rodent-like place cells were only found in the medial pallium of tufted titmice, a food-caching bird. The medial pallium is an avian brain region homologous to the mammalian hippocampus. By contrast, rodent-like head direction cells are found in the medial pallium of quails. Head direction cells are also found in the medial pallium of streaked shearwaters, a migratory bird. The avian hippocampus contains information about the animal's current location or direction, but the neural encoding may differ depending on the ecological characteristics of the bird species. The place cells of bats, which are mammals, fly in three-dimensional space and encode vectorial information toward the goal. Training rats with an ingenious task that required them to choose a direction for each run in a maze suggested that place cells encode a vector for goal-directed spatial navigation. Thus, the scrutiny of the literature on spatial navigation-related neuronal activity across multiple animal species suggests that depending on a combination of external conditions such as the context in which the animal is situated (e.g., the context or the framework composed of landmarks in the environment) and internal conditions such as the ecological and behavioral characteristics of the animal, hippocampal neurons can be identified as place cells or head direction cells. We thus propose a conjecture that primitively, the hippocampus, or its homolog, contains information about the travel direction and that the emergence of the hippocampus during evolution has enabled the generation of vector information to the goal for advanced spatial navigation such as the search for the shortcut path and episodic memory capacity.