دورية أكاديمية
Decomposition of an odorant in olfactory perception and neural representation.
| العنوان: | Decomposition of an odorant in olfactory perception and neural representation. |
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| المؤلفون: | Ye Y; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.; Institute of Psychology, School of Public Affairs, Xiamen University, Xiamen, China., Wang Y; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China.; School of Psychology, Northwest Normal University, Lanzhou, China., Zhuang Y; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China., Tan H; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China., Zuo Z; State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China.; Institute of Artificial Intelligence, Hefei Comprehensive National Science Center, Hefei, China.; Sino-Dannish College, University of Chinese Academy of Sciences, Beijing, China., Yun H; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China., Yuan K; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China., Zhou W; State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China. zhouw@psych.ac.cn.; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China. zhouw@psych.ac.cn.; Chinese Institute for Brain Research, Beijing, China. zhouw@psych.ac.cn. |
| المصدر: | Nature human behaviour [Nat Hum Behav] 2024 Jun; Vol. 8 (6), pp. 1150-1162. Date of Electronic Publication: 2024 Mar 18. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer Nature Publishing Country of Publication: England NLM ID: 101697750 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2397-3374 (Electronic) Linking ISSN: 23973374 NLM ISO Abbreviation: Nat Hum Behav Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: [London] : Springer Nature Publishing, [2017]- |
| مواضيع طبية MeSH: | Olfactory Perception*/physiology , Odorants*, Humans ; Adult ; Male ; Female ; Young Adult ; Magnetic Resonance Imaging ; Piriform Cortex/physiology ; Amygdala/physiology ; Amygdala/diagnostic imaging ; Smell/physiology |
| مستخلص: | Molecules-the elementary units of substances-are commonly considered the units of processing in olfactory perception, giving rise to undifferentiated odour objects invariant to environmental variations. By selectively perturbing the processing of chemical substructures with adaptation ('the psychologist's microelectrode') in a series of psychophysical and neuroimaging experiments (458 participants), we show that two perceptually distinct odorants sharing part of their structural features become significantly less discernible following adaptation to a third odorant containing their non-shared structural features, in manners independent of olfactory intensity, valence, quality or general olfactory adaptation. The effect is accompanied by reorganizations of ensemble activity patterns in the posterior piriform cortex that parallel subjective odour quality changes, in addition to substructure-based neural adaptations in the anterior piriform cortex and amygdala. Central representations of odour quality and the perceptual outcome thus embed submolecular structural information and are malleable by recent olfactory encounters. (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.) |
| References: | Mozell, M. M. & Jagodowicz, M. Chromatographic separation of odorants by the nose: retention times measured across in vivo olfactory mucosa. Science 181, 1247–1249 (1973). (PMID: 4542192) Malnic, B., Godfrey, P. A. & Buck, L. B. The human olfactory receptor gene family. Proc. Natl Acad. Sci. USA 101, 2584–2589 (2004). (PMID: 14983052356993) Amoore, J. E. Stereochemical theory of olfaction. Nature 198, 271–272 (1963). (PMID: 14012641) Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713–723 (1999). (PMID: 10089886) Del Marmol, J., Yedlin, M. A. & Ruta, V. The structural basis of odorant recognition in insect olfactory receptors. Nature 597, 126–131 (2021). (PMID: 343492608410599) Khan, A. G., Thattai, M. & Bhalla, U. S. Odor representations in the rat olfactory bulb change smoothly with morphing stimuli. Neuron 57, 571–585 (2008). (PMID: 183044862258318) Soucy, E. R., Albeanu, D. F., Fantana, A. L., Murthy, V. N. & Meister, M. Precision and diversity in an odor map on the olfactory bulb. Nat. Neurosci. 12, 210–220 (2009). (PMID: 19151709) Mori, K. & Sakano, H. How is the olfactory map formed and interpreted in the mammalian brain? Annu. Rev. Neurosci. 34, 467–499 (2011). (PMID: 21469960) Ma, L. et al. Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb. Proc. Natl Acad. Sci. USA 109, 5481–5486 (2012). (PMID: 224316053325716) Barnes, D. C., Hofacer, R. D., Zaman, A. R., Rennaker, R. L. & Wilson, D. A. Olfactory perceptual stability and discrimination. Nat. Neurosci. 11, 1378–1380 (2008). (PMID: 189787812682180) Pashkovski, S. L. et al. Structure and flexibility in cortical representations of odour space. Nature 583, 253–258 (2020). (PMID: 326122307450987) Gottfried, J. A. Central mechanisms of odour object perception. Nat. Rev. Neurosci. 11, 628–641 (2010). (PMID: 207001423722866) Stettler, D. D. & Axel, R. Representations of odor in the piriform cortex. Neuron 63, 854–864 (2009). (PMID: 19778513) Bekkers, J. M. & Suzuki, N. Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci. 36, 429–438 (2013). (PMID: 23648377) Snitz, K. et al. Predicting odor perceptual similarity from odor structure. PLoS Comput. Biol. 9, e1003184 (2013). (PMID: 240688993772038) Keller, A. et al. Predicting human olfactory perception from chemical features of odor molecules. Science 355, 820–826 (2017). (PMID: 282199715455768) Licon, C. C. et al. Chemical features mining provides new descriptive structure–odor relationships. PLoS Comput. Biol. 15, e1006945 (2019). (PMID: 310221806504111) Wilson, D. A. & Stevenson, R. J. The fundamental role of memory in olfactory perception. Trends Neurosci. 26, 243–247 (2003). (PMID: 12744840) Giessel, A. J. & Datta, S. R. Olfactory maps, circuits and computations. Curr. Opin. Neurobiol. 24, 120–132 (2014). (PMID: 24492088) Saha, D. et al. A spatiotemporal coding mechanism for background-invariant odor recognition. Nat. Neurosci. 16, 1830–1839 (2013). (PMID: 24185426) Nizampatnam, S., Zhang, L., Chandak, R., Li, J. & Raman, B. Invariant odor recognition with ON-OFF neural ensembles. Proc. Natl Acad. Sci. USA 119, e2023340118 (2022). (PMID: 349968678764697) Gottfried, J. A. Function follows form: ecological constraints on odor codes and olfactory percepts. Curr. Opin. Neurobiol. 19, 422–429 (2009). (PMID: 196714932761641) Frisby, J. P. Seeing: Illusion, Brain and Mind (Oxford Univ. Press, 1979). Carhart, R. E., Smith, D. H. & Venkataraghavan, R. Atom pairs as molecular features in structure–activity studies: definition and applications. J. Chem. Inf. Comput. Sci. 25, 64–73 (1985). Cao, Y., Jiang, T. & Girke, T. A maximum common substructure-based algorithm for searching and predicting drug-like compounds. Bioinformatics 24, i366–i374 (2008). (PMID: 185867362718661) Dravnieks, A. Odor quality: semantically generated multidimensional profiles are stable. Science 218, 799–801 (1982). (PMID: 7134974) Secundo, L. et al. Individual olfactory perception reveals meaningful nonolfactory genetic information. Proc. Natl Acad. Sci. USA 112, 8750–8755 (2015). (PMID: 261008654507195) Nara, K., Saraiva, L. R., Ye, X. & Buck, L. B. A large-scale analysis of odor coding in the olfactory epithelium. J. Neurosci. 31, 9179–9191 (2011). (PMID: 216973693758579) Powell, T. P., Cowan, W. M. & Raisman, G. The central olfactory connexions. J. Anat. 99, 791–813 (1965). (PMID: 58671691270719) Carmichael, S. T., Clugnet, M. C. & Price, J. L. Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346, 403–434 (1994). (PMID: 7527806) Lascano, A. M., Hummel, T., Lacroix, J. S., Landis, B. N. & Michel, C. M. Spatio-temporal dynamics of olfactory processing in the human brain: an event-related source imaging study. Neuroscience 167, 700–708 (2010). (PMID: 20153813) Iannilli, E., Wiens, S., Arshamian, A. & Seo, H. S. A spatiotemporal comparison between olfactory and trigeminal event-related potentials. NeuroImage 77, 254–261 (2013). (PMID: 23298751) Gottfried, J. A., Winston, J. S. & Dolan, R. J. Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49, 467–479 (2006). (PMID: 16446149) Li, W., Howard, J. D., Parrish, T. B. & Gottfried, J. A. Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319, 1842–1845 (2008). (PMID: 183691492756335) Howard, J. D., Plailly, J., Grueschow, M., Haynes, J. D. & Gottfried, J. A. Odor quality coding and categorization in human posterior piriform cortex. Nat. Neurosci. 12, 932–938 (2009). (PMID: 194836882834563) Sosulski, D. L., Bloom, M. L., Cutforth, T., Axel, R. & Datta, S. R. Distinct representations of olfactory information in different cortical centres. Nature 472, 213–216 (2011). (PMID: 214515253354569) Kadohisa, M. & Wilson, D. A. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc. Natl Acad. Sci. USA 103, 15206–15211 (2006). (PMID: 170057271622801) Zelano, C., Mohanty, A. & Gottfried, J. A. Olfactory predictive codes and stimulus templates in piriform cortex. Neuron 72, 178–187 (2011). (PMID: 219823783190127) Kriegeskorte, N. & Kievit, R. A. Representational geometry: integrating cognition, computation, and the brain. Trends Cogn. Sci. 17, 401–412 (2013). (PMID: 238764943730178) Turin, L. A spectroscopic mechanism for primary olfactory reception. Chem. Senses 21, 773–791 (1996). (PMID: 8985605) Rubin, B. D. & Katz, L. C. Spatial coding of enantiomers in the rat olfactory bulb. Nat. Neurosci. 4, 355–356 (2001). (PMID: 11276223) Chastrette, M. in Olfaction, Taste, and Cognition (eds Rouby, C. et al.) 100–116 (Cambridge Univ. Press, 2002). Skaggs, E. B. Atomism versus Gestaltism in perception. Psychol. Rev. 47, 347–354 (1940). Moncrieff, R. W. Olfactory adaptation and odour likeness. J. Physiol. 133, 301–316 (1956). (PMID: 133580731359088) Cain, W. S. Odor intensity after self-adaptation and cross-adaptation. Percept. Psychophys. 7, 271–275 (1970). Cain, W. S. & Polak, E. H. Olfactory adaptation as an aspect of odor similarity. Chem. Senses 17, 481–491 (1992). Pierce, J. D. Jr, Zeng, X. N., Aronov, E. V., Preti, G. & Wysocki, C. J. Cross-adaptation of sweaty-smelling 3-methyl-2-hexenoic acid by a structurally-similar, pleasant-smelling odorant. Chem. Senses 20, 401–411 (1995). (PMID: 8590025) Pierce, J. D. Jr, Wysocki, C. J., Aronov, E. V., Webb, J. B. & Boden, R. M. The role of perceptual and structural similarity in cross-adaptation. Chem. Senses 21, 223–237 (1996). (PMID: 8670701) Gori, M., Giuliana, L., Sandini, G. & Burr, D. Visual size perception and haptic calibration during development. Dev. Sci. 15, 854–862 (2012). (PMID: 23106739) Thompson, R. in International Encyclopedia of the Social and Behavioral Sciences (eds Smelser, N. J. & Baltes, P. B.) 6458–6462 (Pergamon, 2001). Pellegrino, R., Sinding, C., de Wijk, R. A. & Hummel, T. Habituation and adaptation to odors in humans. Physiol. Behav. 177, 13–19 (2017). (PMID: 28408237) Li, W., Luxenberg, E., Parrish, T. & Gottfried, J. A. Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52, 1097–1108 (2006). (PMID: 171784111779760) Mori, K., Takahashi, Y. K., Igarashi, K. M. & Yamaguchi, M. Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86, 409–433 (2006). (PMID: 16601265) Fournel, A., Ferdenzi, C., Sezille, C., Rouby, C. & Bensafi, M. Multidimensional representation of odors in the human olfactory cortex. Hum. Brain Mapp. 37, 2161–2172 (2016). (PMID: 269910446867239) Chu, M. W., Li, W. L. & Komiyama, T. Balancing the robustness and efficiency of odor representations during learning. Neuron 92, 174–186 (2016). (PMID: 276670055061050) Kass, M. D., Guang, S. A., Moberly, A. H. & McGann, J. P. Changes in olfactory sensory neuron physiology and olfactory perceptual learning after odorant exposure in adult mice. Chem. Senses 41, 123–133 (2016). (PMID: 26514410) Tsukahara, T. et al. A transcriptional rheostat couples past activity to future sensory responses. Cell 184, 6326–6343 e6332 (2021). (PMID: 348792318758202) Farkhooi, F., Froese, A., Muller, E., Menzel, R. & Nawrot, M. P. Cellular adaptation facilitates sparse and reliable coding in sensory pathways. PLoS Comput. Biol. 9, e1003251 (2013). (PMID: 240981013789775) Patterson, C. A., Wissig, S. C. & Kohn, A. Adaptation disrupts motion integration in the primate dorsal stream. Neuron 81, 674–686 (2014). (PMID: 245071983955163) Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A. & Wachowiak, M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat. Neurosci. 10, 631–639 (2007). (PMID: 17450136) Kermen, F. et al. Molecular complexity determines the number of olfactory notes and the pleasantness of smells. Sci. Rep. 1, 206 (2011). (PMID: 223557213244502) Roblin, D. G. & Eccles, R. Normal range for nasal partitioning of airflow determined by nasal spirometry in 100 healthy subjects. Am. J. Rhinol. 17, 179–183 (2003). (PMID: 12962185) Mai, J. K., Paxinos, G. & Voss, T. Atlas of the Human Brain 3rd edn (Academic Press, 2008). Eickhoff, S. B. et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25, 1325–1335 (2005). (PMID: 15850749) Gottfried, J. A. & Zald, D. H. On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res. Brain Res. Rev. 50, 287–304 (2005). (PMID: 16213593) |
| معلومات مُعتمدة: | 2021ZD0204200 Ministry of Science and Technology of the People's Republic of China (Chinese Ministry of Science and Technology); JCTD-2021-06 Chinese Academy of Sciences (CAS); 2021091 Chinese Academy of Sciences (CAS); YSBR-068 Chinese Academy of Sciences (CAS); 31830037 National Natural Science Foundation of China (National Science Foundation of China); 32000789 National Natural Science Foundation of China (National Science Foundation of China) |
| تواريخ الأحداث: | Date Created: 20240319 Date Completed: 20240625 Latest Revision: 20240625 |
| رمز التحديث: | 20240626 |
| DOI: | 10.1038/s41562-024-01849-0 |
| PMID: | 38499771 |
| قاعدة البيانات: | MEDLINE |
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Full Text Finder | تدمد: | 2397-3374 |
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| DOI: | 10.1038/s41562-024-01849-0 |