Current Biology
Dispatches 15. Peelle, J.E., Gross, J., and Davis, M.H. (2013). Phase-locked responses to speech in human auditory cortex are enhanced during comprehension. Cereb. Cortex 23, 1378–1387. 16. Lakatos, P., Karmos, G., Mehta, A.D., Ulbert, I., and Schroeder, C.E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110–113.
17. Arnal, L.H., Wyart, V., and Giraud, A.L. (2011). Transitions in neural oscillations reflect prediction errors generated in audiovisual speech. Nat. Neurosci. 14, 797–801. 18. Herrmann, C.S., Rach, S., Neuling, T., and Stru¨ber, D. (2013). Transcranial alternating current stimulation: a review of the underlying
mechanisms and modulation of cognitive processes. Front. Hum. Neurosci. 7, 279. 19. Ali, M.M., Sellers, K.K., and Fro¨hlich, F. (2013). Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J. Neurosci. 33, 11262– 11275.
Human Olfaction: It Takes Two Villages Jonas K. Olofsson1,2 and Donald A. Wilson2,3
€g 9A, SE-11419 Stockholm, Sweden of Psychology, Stockholm University, Frescati Hagva & Adolescent Psychiatry, New York University School of Medicine, 1 Park Avenue, New York, NY 10016, USA 3Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, NY 10962, USA Correspondence:
[email protected] (J.K.O.),
[email protected] (D.A.W.) https://doi.org/10.1016/j.cub.2017.12.016 1Department 2Child
Human olfaction is sensitive but poorly encoded by language. A new study comparing horticulturalists and hunter-gatherers suggests that the strength of odor language is dependent on life-style. This work may stimulate olfactory research at the crossroads between biology and culture. Historically, human olfaction has been considered an underdeveloped sense. However, experts now consider the human capacity for detecting and discriminating odors to be excellent [1,2]. Nonetheless, we often struggle to bridge the gap between an initial olfactory impression and a meaningful experience: What is that smell? Is it harmful? How can I describe it to others? Was it you or Sparky? Our shortcomings may be blamed on lifestyle, as many cultures prioritize communication about audiovisual, rather than olfactory, events [3]. However, as recently as the 18–19th century, medical practitioners would often obtain distinct disease cues by smelling their patients [4]. ‘‘Its smell is commonly faint and peculiar, sometimes resembling sweet whey or milk’’, surgeon Herbert Mayo wrote in 1832 about diabetic urine [5]. Olfaction was a method of diagnosing diseases, for example diphtheria (sweet), scurvy (putrid) and scrofula (stale beer) [6]. Olfactory diagnostics fell out of favor as textbooks, rather than close apprenticeships, became primary sources of medical education. Despite valiant efforts by Dr. Mayo and others, olfactory diagnoses defied lexical translation, and required the teacher and the student to smell the same
patient. Our difficulty in communicating olfactory experiences can render them elusive and personal. Conversely, the training of perfumers or wine experts critically involves developing an adequate vocabulary [7]. In this issue of Current Biology, Asifa Majid and Nicole Kruspe [8] provide new evidence for how culture may determine odor language. Asifa Majid and her colleagues have long advocated for the utility of crosscultural approaches to understand the human mind. Olfactory language, being under-recognized in the West, may be a particularly fruitful venue. Previously, this lab showed that the Jahai, a group of hunter-gatherers in the Malay Peninsula, are more consistent in naming smells — but not colors — compared to participants in the Netherlands [9]. In their recent work, Majid and Kruspe [8] provide new evidence suggesting that subsistence mode, specifically, hunting and gathering, might be a decisive cultural factor in developing a robust odor vocabulary. They studied two proximate populations in their home villages in the Malay Peninsula; the Semaq Beri, a nomadic hunter-gatherer group, and the Semelai (Figure 1), who use slash-andburn agriculture. Members of these
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populations speak closely related languages in the Aslian language family and have similar physical features. The researchers presented odors from a set commonly used to assess olfactory abilities [10]. The participants’ responses were transcribed in order to create two variables of key interest: the agreement between different individuals on how to describe an odor, and whether the responses were source-based (e.g., described based on where the odor originated from, such as an orange or a rose), evaluative (e.g., such as pleasant or strong) or abstract. As a control condition, the researchers asked the participants to describe colors. There were clear group differences: the agricultural Semelai, similar to wellstudied psychology undergraduates, used primarily source-based descriptors for odors (but not colors) and were less consistent than the hunter-gatherer Semaq Beri, who used abstract terms. Majid and Kruspe [8] thus convincingly argue that culture shapes our olfactory language capabilities. Their work highlights topics of broad theoretical interest in the behavioral and brain sciences; below, we discuss how it may impact the field of olfaction in the coming years.
Current Biology
Dispatches The work by Majid and Kruspe [8] provides a refreshing approach to olfactory science, which has been characterized by a rather one-sided focus on the molecular determinants of olfactory perception, while important roles of memory and language have been overlooked. As a consequence, we still know little about how cognitive systems interact with olfactory sensations. Although the English language has a wealth of terms used to describe smells, these words appear insufficient to reliably communicate olfactory experiences. Many odor-associated terms are sourcebased and they apply only to very specific odors, for example ‘cherry’ or ‘orange’, but are useless in all other cases. Other odor-associated terms apply more broadly, for example ‘heavy’ and ‘light’, but there is little agreement on which odors they describe [11]. The world of scent does not adhere to general category concepts by which we neatly divide the world. In contrast, the Semaq Beri and Jahai use designated abstract terms for broad odor categories. For example, the word Chεs describes to the Jahai the smell of petrol, smoke, bat droppings and bat caves, some species of millipede, root of wild ginger, leaf of gingerwort, wood of wild mango, among other odor sources [8]. Such terms, unlike ‘heavy’ or ‘light’, are not on lease from other sensory systems. The effects of such olfactory vocabulary need further investigation. The notion that language shapes our experiences is a long-standing and controversial hypothesis since popularized in the 1930s by Benjamin Lee Whorf and Edward Sapir. The SapirWhorf hypothesis holds that even basic sensory discrimination is influenced by language concepts. Some evidence does in fact indicate that the differentiation of close-to-identical color patches is easier if these colors are are on opposite sides of a linguistic boundary, for example a bluish green versus a greenish blue [12]. In olfaction, access to odor labels is known to facilitate identification [13]. Majid and Kruspe [8] elegantly link olfaction to a long-standing tradition in anthropology and linguistics, which might inspire new and innovative olfactory language experiments. Although visual objects may have a color, as well as an odor, it is not clear that
Figure 1. On odor terms. Semelai speaker with Nicole Kruspe discussing odor. Image: Noah Azman.
colors and odors, the two stimulus types used by Majid and Kruspe [7], make for the best analogy. For example, while colors are decoded by only three receptor types in humans, there are hundreds of odorant receptors, and their ensemble of coding characteristics makes it harder to reduce odor perception to a few dimensions. A current framework holds instead that familiar odors are processed as perceptual ‘objects’ [14,15], similar to how combinations of visual features are perceived as objects. Specifically, most odors are mixtures of many different molecules. For example, the odor of an orange has around one-hundred different volatile molecules, most of which have an odor themselves if smelled alone. Despite this complexity, given experience with oranges, we merge those different molecular features into a perceptual whole [15], which we may then verbally label as ‘orange’. Learning and experience play crucial roles in this process, allowing the olfactory system to learn which molecular features tend to cooccur to form neural templates of those combinations [16]. In this way, active olfactory training or cultural imposition may not only shape olfactory language but actually shape odor perception. The work by Majid and Kruspe [8] highlights how cultural differences may be harnessed for insights into evolutionary constraints and cultural/experienceinduced plasticity. The repertoire of olfactory receptor genes is highly diverse across species and individuals, and olfactory receptor variants can contribute to unique olfactory experiences [17]. An
important aspect of the work by Majid and Kruspe [8] is thus the presumed genetic similarity of the Semelai and Semaq Beri, making genetic group differences unlikely to influence the present results. Furthermore, exposure to pollution may compromise the olfactory abilities of urban residents, but are unlikely to play a major role here [18]. A recent theoretical framework holds that the inability to name objects based on their olfactory, as opposed to their visual, appearance may be explained by the brain circuitry involved in associating olfactory (the smell of a cherry) and visual (the picture of a cherry) object features to lexico-semantic representations [19]. The cherry odor may enable less distinctive features (sweet, fruity) than its visual counterpart (small, round, dark red, has a stem) before the object is mapped onto a source name via designated sensoryspecific language hubs [20]. Just as the limited olfactory feature extraction may be explained by physiology, presumably the association between odor percepts and language representations may be limited by cortical networks. Controlled intervention studies might reveal how these limitations are challenged by experience. If odor naming capacity is profoundly shaped by cultural experience, deterministic notions about strict biological limitations in the olfactory system are put into question. But explanations invoking physiology do not exclude important roles for culture and plasticity. Rather, sensory and cognitive systems are best characterized as
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Current Biology
Dispatches biological systems that develop under genetic as well as environmental influence. The precise bio-cultural interactions needed to develop the extraordinary olfactory capabilities observed in these hunter-gatherer populations, and assessing when and how these conditions are met, are largescale issues to be addressed by future research. The study by Majid and Kruspe [8], together with new developments in sensory plasticity, genetics and cognition, may thus pave the way for exciting new explorations of olfaction at the crossroad between biology and culture.
4. Palmer, R. (1993). In bad odour: smell and its significance in medicine from antiquity to the seventeenth century. In Medicine and the Five Senses, W.F. Bynum, and R. Porter, eds. (New York: Cambridge University Press), pp. 61–68. 5. Lakhtakia, R. (2014). Twist of taste: gastronomic allusions in medicine. Med. Humanit. 40, 117–118. 6. Hayden, G.F. (1980). Olfactory diagnosis in medicine. Postgrad Med. 67, 110–115, 118. 7. Royet, J.P., Plailly, J., Saive, A.L., Veyrac, A., and Delon-Martin, C. (2013). The impact of expertise in olfaction. Front. Psychol. 4, 928. 8. Majid, A., and Kruspe, N. (2018). Huntergatherer olfaction is special. Curr. Biol. 28, 409–413. 9. Majid, A., and Burenhult, N. (2014). Odors are expressible in language, as long as you speak the right language. Cognition 130, 266–270.
lateralized effect of language on preattentive categorical perception of color. Proc. Natl. Acad. Sci. USA 108, 14026–14030. 13. Cain, W.S. (1979). To know with the nose: keys to odor identification. Science 203, 467–470. 14. Gottfried, J.A. (2010). Central mechanisms of odour object perception. Nat. Rev. Neurosci. 11, 628–641. 15. Wilson, D.A., and Stevenson, R.J. (2003). The fundamental role of memory in olfactory perception. Trends Neurosci. 26, 243–247. 16. Chapuis, J., and Wilson, D.A. (2012). Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat. Neurosci. 15, 155–161. 17. Keller, A., Zhuang, H., Chi, Q., Vosshall, L.B., and Matsunami, H. (2007). Genetic variation in a human odorant receptor alters odour perception. Nature 449, 468–472.
REFERENCES 1. McGann, J.P. (2017). Poor human olfaction is a 19th-century myth. Science 356, eaam7263. 2. Laska, M. (2017). Human and animal olfactory capabilities compared. In Springer Handbook of Odors, A. Buettner, ed. (New York: Springer), pp. 81–92. 3. San Roque, L., Kendrick, K.H., Norcliffe, E., Brown, P., Defina, R., Dingemanse, M., Dirksmeyer, T., Enfield, N.J., Floyd, S., Hammond, J., et al. (2015). Vision verbs dominate in conversation across cultures, but the ranking of non-visual verbs varies. Cognitive Linquistics 26, 31–60.
10. Hummel, T., Kobal, G., Gudziol, H., and Mackay-Sim, A. (2007). Normative data for the ‘‘Sniffin’ Sticks’’ including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur. Arch. Otorhinolaryngol. 264, 237–243. 11. Iatropoulos, G., Herman, P.A., Lansner, A., Karlgren, J., Larsson, M., and Olofsson, J.K. (2017). The language of smell: Connecting linguistic and psychophysical properties of odor descriptors. Retrieved from psyarxiv. com/bg6t8. 12. Mo, L., Xu, G., Kay, P., and Tan, L.H. (2011). Electrophysiological evidence for the left-
18. Sorokowska, A., Sorokowski, P., Hummel, T., and Huanca, T. (2013). Olfaction and environment: Tsimane’ of Bolivian rainforest have lower threshold of odor detection than industrialized German people. PLoS One 8, e69203. 19. Olofsson, J.K., and Gottfried, J.A. (2015). The muted sense: neurocognitive limitations of olfactory language. Trends Cogn. Sci. 19, 314–321. 20. Olofsson, J.K., Hurley, R.S., Bowman, N.E., Bao, X., Mesulam, M.M., and Gottfried, J.A. (2014). A designated odor-language integration system in the human brain. J. Neurosci. 34, 14864–14873.
Carbon Fixation: ‘‘Let Things Flow Naturally Forward in Whatever Way They Like’’ Wolfgang Nitschke
nerge tique et Inge nierie des Prote ines (BIP) UMR 7281, IMM FR3479, CNRS/Aix-Marseille University, Marseille, France Laboratoire de Bioe Correspondence:
[email protected] https://doi.org/10.1016/j.cub.2017.12.039
Mixed-acid fermentation generates H2 and CO2 from formate. As shown in a recent study, the formate oxidation reaction can be driven backwards when sufficiently high partial pressures of the gases are applied, suggesting potentially interesting biotechnological applications. Escherichia coli grown in the presence of glucose — but in the absence of electron acceptors — ferments the sugar to a mix of organic acids; specifically, lactic, succinic and formic acids. The formic acid produced in this ‘mixed-acid fermentation’ is further reacted with protons to yield two gases,
CO2 and H2. In this redox process, the electrons derived from the oxidation of formate to CO2 are used for the reduction of two protons to yield molecular hydrogen. Oxidising formate to CO2 (which escapes into the gas phase) by using ubiquitously available protons as electron acceptors is a
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clever way to prevent the main fermentation reaction from stalling due to product inhibition. All this was elucidated almost a century ago [1,2], and the process has since become a standard entry in textbooks on microbial physiology. As a sorted-out mechanism, it was further studied only by a fringe