Poor human olfaction is a 19th-century myth
TL;DR: 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.
Abstract: 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.
Citations
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Abstract: Turmerones (α-turmerone, β-turmerone, and ar-turmerone) are the major volatile compounds in turmeric (Curcuma longa), a perennial herb of the ginger family. We previously reported that inhaled volatile turmerones could be transferred in the blood and organs. However, the difference between the two pathways, oral administration and inhalation, and the effect of inhaled turmerones on biological activities remain unknown. In this study, we compared the distribution patterns of turmerones after oral administration and inhalation. The relative levels (concentrations of turmerones in each organ/serum) in the lung, olfactory bulb, brain, heart, kidney, and epididymal fat in the inhalation group tended to be, or are significantly, higher than in the oral administration group. The relative levels of brown adipose tissue in the inhalation group were lower than in the oral administration group. Long-term (50 days) inhalation to volatile turmerones suppressed weight gain and hypertrophy of adipocytes in the epididymal fat of mice fed a high-fat diet. These results suggest that inhaled turmerones can be incorporated into the organs of mice via different pathway from as to those from oral administration and can affect the biological function of the organs under certain conditions.
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Abstract: Anthropogenic disruptions to animal sensory ecology are as old as our species. But what about the effect on human sensory ecology? Human sensory dysfunction is increasing globally at great economic and health costs (mental, physical, and social). Contemporary sensory problems are directly tied to human behavioral changes and activity as well as anthropogenic pollution. The evolutionary sensory ecology and anthropogenic disruptions to three human senses (vision, audition, olfaction) are examined along with the economic and health costs of functionally reduced senses and demographic risk factors contributing to impairment. The primary goals of the paper are (a) to sew an evolutionary and ecological thread through clinical narratives on sensory dysfunction that highlights the impact of the built environment on the senses, and (b) to highlight structural, demographic, and environmental injustices that create sensory inequities in risk and that promote health disparities.
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Abstract: Prion diseases, or transmissible spongiform encephalopathies (TSEs), are a class of fatal neurodegenerative diseases caused by the entry and spread of infectious prion proteins (PrPSc) in the central nervous system (CNS). These diseases are endemic to certain mammalian animal species that use their sense of smell for a variety of purposes and therefore expose their nasal cavity (NC) to PrPSc in the environment. Prion diseases that affect humans are either inherited due to a mutation of the gene that encodes the prion protein, acquired by exposure to contaminated tissues or medical devices, or develop without a known cause (referred to as sporadic). The purpose of this review is to identify components of the NC that are involved in prion transport and to summarize the evidence that the NC serves as a route of entry (centripetal spread) and/or a source of shedding (centrifugal spread) of PrPSc, and thus plays a role in the pathogenesis of the TSEs.
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References
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TL;DR: The present data suggest specific changes of individual olfactory functions in relation to age, with odor thresholds declining most dramatically compared to odor discrimination and odor identification.
Abstract: "Sniffin' Sticks" is a test of nasal chemosensory function that is based on pen-like odor dispensing devices, introduced some 10 years ago by Kobal and co-workers. It consists of tests for odor threshold, discrimination, and identification. Previous work established its test-retest reliability and validity. Results of the test are presented as "TDI score", the sum of results obtained for threshold, discrimination, and identification measures. While normative data have been established they are based on a relatively small number of subjects, especially with regard to subjects older than 55 years where data from only 30 healthy subjects have been used. The present study aimed to remedy this situation. Now data are available from 3,282 subjects as compared to data from 738 subjects published previously. Disregarding sex-related differences, the TDI score at the tenth percentile was 24.9 in subjects younger than 15 years, 30.3 for ages from 16 to 35 years, 27.3 for ages from 36 to 55 years, and 19.6 for subjects older than 55 years. Because the tenth percentile has been defined to separate hyposmia from normosmia, these data can be used as a guide to estimate individual olfactory ability in relation to subject's age. Absolute hyposmia was defined as the tenth percentile score of 16-35 year old subjects. Other than previous reports the present norms are also sex-differentiated with women outperforming men in the three olfactory tests. Further, the present data suggest specific changes of individual olfactory functions in relation to age, with odor thresholds declining most dramatically compared to odor discrimination and odor identification.
1,266 citations
TL;DR: Differential activity in amygdala and orbitofrontal cortex encodes the current value of reward representations accessible to predictive cues, and responses evoked by a predictive target stimulus were decreased after devaluation, whereas responses to the nondevalued stimulus were maintained.
Abstract: Adaptive behavior is optimized in organisms that maintain flexible representations of the value of sensory-predictive cues. To identify central representations of predictive reward value in humans, we used reinforcer devaluation while measuring neural activity with functional magnetic resonance imaging. We presented two arbitrary visual stimuli, both before and after olfactory devaluation, in a paradigm of appetitive conditioning. In amygdala and orbitofrontal cortex, responses evoked by a predictive target stimulus were decreased after devaluation, whereas responses to the nondevalued stimulus were maintained. Thus, differential activity in amygdala and orbitofrontal cortex encodes the current value of reward representations accessible to predictive cues.
1,137 citations
TL;DR: Analysis of data collected on 131 species of primates, bats, and insectivores showed that the sizes of brain components, from medulla to forebrain, are highly predictable from absolute brain size by a nonlinear function.
Abstract: Analysis of data collected on 131 species of primates, bats, and insectivores showed that the sizes of brain components, from medulla to forebrain, are highly predictable from absolute brain size by a nonlinear function. The order of neurogenesis was found to be highly conserved across a wide range of mammals and to correlate with the relative enlargement of structures as brain size increases, with disproportionately large growth occurring in late-generated structures. Because the order of neurogenesis is conserved, the most likely brain alteration resulting from selection for any behavioral ability may be a coordinated enlargement of the entire nonolfactory brain.
1,123 citations
TL;DR: Human ORs cover a similar 'receptor space' as the mouse ORs, suggesting that the human olfactory system has retained the ability to recognize a broad spectrum of chemicals even though humans have lost nearly two-thirds of the OR genes as compared to mice.
Abstract: Olfactory receptor (OR) genes are the largest gene superfamily in vertebrates. We have identified the mouse OR genes from the nearly complete Celera mouse genome by a comprehensive data mining strategy. We found 1,296 mouse OR genes (including ∼20% pseudogenes), which can be classified into 228 families. OR genes are distributed in 27 clusters on all mouse chromosomes except 12 and Y. One OR gene cluster matches a known locus mediating a specific anosmia, indicating the anosmia may be due directly to the loss of receptors. A large number of apparently functional 'fish-like' Class I OR genes in the mouse genome may have important roles in mammalian olfaction. Human ORs cover a similar 'receptor space' as the mouse ORs, suggesting that the human olfactory system has retained the ability to recognize a broad spectrum of chemicals even though humans have lost nearly two-thirds of the OR genes as compared to mice.
899 citations
TL;DR: The presence of a human RMS is demonstrated, which is unexpectedly organized around a lateral ventricular extension reaching the OB, and the neuroblasts in it are illustrated.
Abstract: The rostral migratory stream (RMS) is the main pathway by which newly born subventricular zone cells reach the olfactory bulb (OB) in rodents. However, the RMS in the adult human brain has been elusive. We demonstrate the presence of a human RMS, which is unexpectedly organized around a lateral ventricular extension reaching the OB, and illustrate the neuroblasts in it. The RMS ensheathing the lateral olfactory ventricular extension, as seen by magnetic resonance imaging, cell-specific markers, and electron microscopy, contains progenitor cells with migratory characteristics and cells that incorporate 5-bromo-2'-deoxyuridine and become mature neurons in the OB.
881 citations