Abstract
To make maps from airborne odours 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 limbic system evolution offer a framework to understand why this occurs. The answer begins with the evolution of nasal respiration in Devonian lobe-finned fishes. 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 was accompanied by a loss of hippocampal structure (whales) and an absence of hippocampal theta oscillations during navigation (bats). In conclusion, models of hippocampal function that are divorced from considerations of ecology and evolution fall short of explaining hippocampal diversity across mammals and even hippocampal function in humans.This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.
Highlights
Models of hippocampal function are derived from intensive study of two rodent species, the laboratory mouse and laboratory rat
Studies of the European hedgehog had already identified the synchronization of theta and respiration, but until, recently, these oscillations were viewed as artefacts to be filtered from recording data [32,35]
Francoise Schenk and I proposed to ‘unpack’ the cognitive map by distinguishing between stimuli that are perceived as gradients or compasses and stimuli perceived as objects [44]
Summary
Models of hippocampal function are derived from intensive study of two rodent species, the laboratory mouse and laboratory rat. The crisis comes from unexpected results that question the hegemony of visual cues in the study of hippocampal function This is a series of prominent studies demonstrating that nasal respiration profoundly influences memory processes, in humans as well as murines [31,32,33,34]. Studies of the European hedgehog had already identified the synchronization of theta and respiration, but until, recently, these oscillations were viewed as artefacts to be filtered from recording data [32,35] This is not a question limited to olfactory structures processing odours, but instead the realization that nasal (but not oral) respiration entrains fundamental processes of cognition. I will argue that only by reconceptualizing hippocampal function can we understand why nasal respiration influences memory and how olfactory and hippocampal functions have radiated and adapted to new challenges, even in our species
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