Of Space and Smell: The Strange Evolution of the Human Nose

We humans are the Cyrano de Bergerac's of the primate world, with conspicuously large external noses compared to other great apes. To understand why our nose evolved we must first understand the function of olfaction. To do this requires traveling back in time to the evolution of the first brain. I will describe the hypothesis that the sense of smell evolved as a sense of direction, playing a critical role in navigation and that this function explains why olfactory systems are so plastic and variable in size across animals. The navigation function of olfaction in humans has been largely neglected and I will describe studies showing that humans can orient accurately to odors in real world and virtual reality environments. But why such a nose? To understand this, I return to an evolutionary framework to describe how the first nose, a structure used both for respiration and olfaction, appeared in air-breathing fish. I describe a new hypothesis (PROUST: perceiving and representing odor utility in space and time) to explain how the evolution of air-breathing could have forced vertebrates to segregate olfactory mapping of space to the main olfactory system and the mapping of odors across time to the newly evolved second (vomeronasal) olfactory system. This dichotomy of function and the subsequent conflict between mapping time versus space using odors, could have led to a number of novel vertebrate solutions to sample odors, including the forked tongue of the snake and the human external nose. I will end by proposing that this perspective on the evolution and function of human olfaction could enhance current paradigms in human-robot communication and decision making.