Poor human olfaction is a 19th-century myth

BACKGROUND It is widely believed that the human sense of smell is inferior to that of other mammals, especially rodents and dogs. This Review traces the scientific history of this idea to 19th-century neuroanatomist Paul Broca. He classified humans as “nonsmellers” not owing to any sensory testing but because he believed that the evolutionary enlargement of the human frontal lobe gave human beings free will at the expense of the olfactory system. He especially emphasized the small size of the human brain’s olfactory bulb relative to the size of the brain overall, and noted that other mammals have olfactory bulbs that are proportionately much larger. Broca’s claim that humans have an impoverished olfactory system (later labeled “microsmaty,” or tiny smell) influenced Sigmund Freud, who argued that olfactory atrophy rendered humans susceptible to mental illness. Humans’ supposed microsmaty led to the scientific neglect of the human olfactory system for much of the 20th century, and even today many biologists, anthropologists, and psychologists persist in the erroneous belief that humans have a poor sense of smell. Genetic and neurobiological data that reveal features unique to the human olfactory system are regularly misinterpreted to underlie the putative microsmaty, and the impact of human olfactory dysfunction is underappreciated in medical practice. ADVANCES Although the human olfactory system has turned out to have some biological differences from that of other mammalian species, it is generally similar in its neurobiology and sensory capabilities. The human olfactory system has fewer functional olfactory receptor genes than rodents, for instance, but the human brain has more complex olfactory bulbs and orbitofrontal cortices with which to interpret information from the roughly 400 receptor types that are expressed. The olfactory bulb is proportionately smaller in humans than in rodents, but is comparable in the number of neurons it contains and is actually much larger in absolute terms. Thus, although the rest of the brain became larger as humans evolved, the olfactory bulb did not become smaller. When olfactory performance is compared experimentally between humans and other animals, a key insight has been that the results are strongly influenced by the selection of odors tested, presumably because different odor receptors are expressed in each species. When an appropriate range of odors is tested, humans outperform laboratory rodents and dogs in detecting some odors while being less sensitive to other odors. Like other mammals, humans can distinguish among an incredible number of odors and can even follow outdoor scent trails. Human behaviors and affective states are also strongly influenced by the olfactory environment, which can evoke strong emotional and behavioral reactions as well as prompting distinct memories. Odor-mediated communication between individuals, once thought to be limited to “lower animals,” is now understood to carry information about familial relationships, stress and anxiety levels, and reproductive status in humans as well, although this information is not always consciously accessible. OUTLOOK The human olfactory system is increasingly understood to be highly dynamic. Olfactory sensitivity and discrimination abilities can be changed by experiences like environmental odor exposure or even just learning to associate odors with other stimuli in the laboratory. The neurobiological underpinnings of this plasticity, including “bottom-up” factors like regulation of peripheral odor receptors and “top-down” factors like the sensory consequences of emotional and cognitive states, are just beginning to be understood. The role of olfactory communication in shaping social interactions is also actively being explored, including the social spread of emotion through olfactory cues. Finally, impaired olfaction can be a leading indicator of certain neurodegenerative diseases, notably Parkinson’s disease and Alzheimer’s disease. New experimentation will be required to understand how olfactory sequelae might also reflect problems elsewhere in the nervous system, including mental disorders with sensory symptomatology. The idea that human smell is impoverished compared to other mammals is a 19th-century myth.