Precise spatial representations in the hippocampus of a food-caching bird

Abstract

The hippocampus is an ancient neural circuit required for the formation of episodic memories. In mammals, this ability is thought to depend on well-documented patterns of neural activity, including place cells and sharp wave ripples. Notably, neither pattern has been found in non-mammals, despite compelling examples of episodic-like memory across a wide range of vertebrates. Does episodic memory nonetheless have a universal implementation across distant neural systems? We addressed this question by recording neural activity in the hippocampus of the tufted titmouse - an intense memory specialist from a food-caching family of birds. These birds cache large numbers of food items at scattered, concealed locations and use hippocampus-dependent memory to retrieve their caches. We found remarkably precise spatial representations akin to classic place cells, as well as sharp wave ripples, in the titmouse hippocampus. These patterns were organized along similar anatomical axes to those found in mammals. In contrast, spatial coding was weaker in a different, non-food-caching bird species. Our findings suggest a striking conservation of hippocampal mechanisms across distant vertebrates, in spite of vastly divergent anatomy and cytoarchitecture. At the same time, these results demonstrate that the exact implementation of such common mechanisms may conform to the unique ethological needs of different species.