The PROUST hypothesis: how the evolution of air breathing shaped hippocampal function

Abstract:
To make maps from air-borne odors requires dynamic respiratory patterns. I propose that this constraint explains the modulation of memory by nasal respiration in mammals, including murine rodents (e.g., laboratory mouse, laboratory rat) and humans. My prior theories of hippocampal evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fish. This evolutionary innovation led to adaptive radiations in chemosensory systems, including the emergence of the vomeronasal system and a specialization of the main olfactory system for spatial orientation. As mammals continued to radiate into environments hostile to spatial olfaction (air, water), there was a loss of hippocampal structure and function in lineages that evolved sensory modalities adapted to these new environments. Hence the independent evolution of echolocation in bats and toothed whales is accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, the standard murine model of hippocampal function, divorced from considerations of ecology and evolution, not only falls short of explaining hippocampal diversity in mammals but cannot even address emerging principles of human memory.

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