Social Place-Cells in the Bat Hippocampus
Science 12 Jan 2018: Vol. 359, Issue 6372, pp. 218-224
Social place-cells in the bat hippocampus
David B. Omer, et.al.
Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel.
Social animals have to know the spatial positions of conspecifics. However, it is unknown how the position of others is represented in the brain. We designed a spatial observational-learning task, in which an observer bat mimicked a demonstrator bat while we recorded hippocampal dorsal-CA1 neurons from the observer bat. A neuronal subpopulation represented the position of the other bat, in allocentric coordinates. About half of these “social place-cells” represented also the observer’s own position—that is, were place cells. The representation of the demonstrator bat did not reflect self-movement or trajectory planning by the observer. Some neurons represented also the position of inanimate moving objects; however, their representation differed from the representation of the demonstrator bat. This suggests a role for hippocampal CA1 neurons in social-spatial cognition.
It is important for social animals to know the spatial position of conspecifics, for purposes of social interactions, observational learning, and group navigation. Decades of research on the mammalian hippocampal formation has revealed a set of spatial neurons that represent self-position and orientation, including place cells, grid cells, head-direction cells, and border/boundary cells. However, it remains unknown how the location of other animals is represented in the brain.
We found in this work a subpopulation of cells in bat dorsal CA1 that encode the position of conspecifics, in allocentric coordinates. This representation could not be explained by self-head-movements or by self-trajectory-planning. The responses to the conspecific were directional, which is in line with the directionality of classical place cells, but can also be interpreted through the social difference between an approaching and receding conspecific. Social place fields are unlikely to reflect either distance-coding (observer-demonstrator distance) or time-coding (time since demonstrator-takeoff) because in both cases, we would expect rather symmetric firing fields on flights to both ball A and ball B, whereas nearly all the social place-cells had a firing field on one side only. However, an alternative interpretation is that these neurons encode a position-by-time signal: Namely, they encode the spatial side to which the demonstrator bat is flying, together with its time from takeoff. We also found qualitative differences between the spatial representations of conspecifics versus inanimate moving objects. The different encoding of conspecifics versus objects may arise from (partially) different mechanisms. For example, spatial representation of moving objects in CA1 might arise from convergence of spatial inputs from grid cells in the medial entorhinal cortex and object-related inputs from neurons in the lateral entorhinal cortex; by contrast, social place-cells may also involve socially modulated inputs from CA2. Future studies are thus needed in order to search for social place-cells in the bat CA2, medial, and lateral entorhinal cortices, as well as in the ventral CA1, which was recently shown to be important for social memory.
It may seem surprising that social place-cells were not discovered previously in several studies of rat hippocampus that looked for a modulation of classical place fields by the presence of conspecifics. We believe that the key difference is in the task: In those previous studies, there was no incentive for the animal to pay attention to the position of the conspecific; our task, in contrast, required the bat to pay close attention to the position of the other bat and to hold this position in memory during a 12.7-s average delay, which revealed a spatial representation for the other. This interpretation is consistent with many studies that showed that hippocampal representations are highly task-dependent, plastic, and memory-dependent. Additionally, this task created a high level of social interactions between the two bats: When the bats were together at the start ball, they often approached and touched each other and emitted many social vocalizations, and this intensely social situation may have contributed to the representation of the conspecific.
There is an apparent similarity between the social place-cells, which encode the position of the other, and “mirror neurons” in monkeys, which encode the actions of the other (One difference, however, is that noncongruent social place-cells are still useful functionally because they encode meaningful information about the position of the other, whereas it is less clear how noncongruent mirror neurons in monkeys might be useful for the proposed functions of mirror neurons. Thus, social place-cells are conceptually different from mirror neurons, although both might possibly share a similar functional principle, whereby the same neuronal circuit can be used for self-representation as well as for representing conspecifics.
Last, we speculate that social place-cells may play a role in a wide range of social behaviors in many species—from group navigation and coordinated hunting to observational learning, social hierarchy, and courtship—and may be relevant also for the representation of nonconspecific animals—for example, for spatial encoding of predators and prey. These results open many questions for future studies: How are multiple animals represented in the brain? Is there a different representation for socially dominant versus subordinate animals, and for males versus females? These and many other questions await investigation in order to elucidate the neural basis of social-spatial cognition.
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