Hippocampus Spatial Representations of Self and Other

 

Science  12 Jan 2018:Vol. 359, Issue 6372, pp. 213-218

Spatial representations of self and other in the hippocampus

Laboratory for Systems Neurophysiology, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan.

Laboratory for Neural Computation and Adaptation, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan.

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An animalís awareness of its location in space depends on the activity of place cells in the hippocampus. How the brain encodes the spatial position of others has not yet been identified. We investigated neuronal representations of other animalsí locations in the dorsal CA1 region of the hippocampus with an observational T-maze task in which one rat was required to observe another ratís trajectory to successfully retrieve a reward. Information reflecting the spatial location of both the self and the other was jointly and discretely encoded by CA1 pyramidal cells in the observer rat. A subset of CA1 pyramidal cells exhibited spatial receptive fields that were identical for the self and the other. These findings demonstrate that hippocampal spatial representations include dimensions for both self and nonself.

Spatial navigation requires the hippocampus. The cognitive map theory states that spatial recognition in the hippocampus is allocentric. Place cells in the hippocampus are the physiological correlate of this representation because they are highly sensitive to changes in landmarks and contexts. The characterization of additional types of navigational representations, including head-direction cells and grid cells, has promoted our understanding of the neural mechanisms of allocentric spatial representations in the hippocampal-entorhinal cortex network. The studies of these neural maps have focused on the animalís own position in space. It still remains unclear whether and how spatial information of nonself, such as the position of conspecifics, landmarks, and moving objects, is represented in the hippocampus.

In the hippocampus, spatial information is encoded not only by the average firing rates of the neurons but also by the timing of the spikes with respect to the phase of the underlying theta oscillations.

We propose an extended model of hippocampal spatial representations that can include dimensions for both self and other. Our model, encompassing various types of spatial representations, can categorize spatial representations into four types: own place fields,†† joint place fields,†† otherís place fields,†† and common place fields. In particular, the common place field could be hypothesized to be a mirror representation of place. Combinatorial representations of spatial information of self and nonself would open the door to examining whether this allocentric spatial representation extends more generally to other nonliving moving objects and how it is generated in the hippocampal-entorhinal cortex network. Our data indicate that the place cells in the hippocampus encode sufficient spatial information for organizing the recognition of other animals, which is essential for social behavior.

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