Altered morphological traits along central olfactory centres in congenitally blind subjects.
congenital blindness
magnetic resonance imaging (MRI)
neuroplasticity
olfactory bulb
olfactory perception
olfactory system
Journal
The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
revised:
28
06
2022
received:
20
01
2022
accepted:
30
06
2022
pubmed:
7
7
2022
medline:
17
8
2022
entrez:
6
7
2022
Statut:
ppublish
Résumé
It is well documented that early sensory loss typically alters brain morphology in the areas associated with the lost sense. However, much less is known about the impact of early sensory loss on the remainder of the sensory regions. Therefore, we investigated whether congenitally blind (CB) individuals show brain alterations in the olfactory system by comparing cortical morphology and olfactory bulb (OB) volume between 16 congenitally blind individuals and 16 sighted matched controls. Our results showed that not only CB blind individuals exhibited smaller OB but also alterations of cortical density in some higher olfactory processing centres, but unchanged cortical thickness. Our current findings suggest that a lifelong absence of visual input leads to morphological alterations in olfactory processing areas.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4486-4500Informations de copyright
© 2022 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
Références
Al Aïn, S., Poupon, D., Hétu, S., Mercier, N., Steffener, J., & Frasnelli, J. (2019). Smell training improves olfactory function and alters brain structure. NeuroImage, 189, 45-54. https://doi.org/10.1016/j.neuroimage.2019.01.008
Alary, F., Goldstein, R., Duquette, M., Chapman, C. E., Voss, P., & Lepore, F. (2008). Tactile acuity in the blind: A psychophysical study using a two-dimensional angle discrimination task. Experimental Brain Research, 187(4), 587-594. https://doi.org/10.1007/s00221-008-1327-7
Anderson, A. K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D. G., Glover, G., Gabrieli, J. D., & Sobel, N. (2003). Dissociated neural representations of intensity and valence in human olfaction. Nature Neuroscience, 6(2), 196-202. https://doi.org/10.1038/nn1001
Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry-The methods. NeuroImage, 11(6), 805-821. https://doi.org/10.1006/nimg.2000.0582
Battal, C., Occelli, V., Bertonati, G., Falagiarda, F., & Collignon, O. (2020). General enhancement of spatial hearing in congenitally blind people. Psychological Science, 31(9), 1129-1139. https://doi.org/10.1177/0956797620935584
Bavelier, D., & Neville, H. J. (2002). Cross-modal plasticity: Where and how? Nature Reviews Neuroscience, 3(6), 443-452. https://doi.org/10.1038/nrn848
Beaulieu-Lefebvre, M., Schneider, F. C., Kupers, R., & Ptito, M. (2011). Odor perception and odor awareness in congenital blindness. Brain Research Bulletin, 84(3), 206-209. https://doi.org/10.1016/j.brainresbull.2010.12.014
Bitter, T., Brüderle, J., Gudziol, H., Burmeister, H. P., Gaser, C., & Guntinas-Lichius, O. (2010). Gray and white matter reduction in hyposmic subjects-A voxel-based morphometry study. Brain Research, 1347, 42-47. https://doi.org/10.1016/j.brainres.2010.06.003
Bitter, T., Gudziol, H., Burmeister, H. P., Mentzel, H. J., Guntinas-Lichius, O., & Gaser, C. (2010). Anosmia leads to a loss of gray matter in cortical brain areas. Chemical Senses, 35(5), 407-415. https://doi.org/10.1093/chemse/bjq028
Botvinick, M. M. (2007). Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function. Cognitive, Affective, & Behavioral Neuroscience, 7(4), 356-366. https://doi.org/10.3758/CABN.7.4.356
Büchel, C. (2003). Cortical hierarchy turned on its head. Nature Neuroscience, 6(7), 657-658. https://doi.org/10.1038/nn0703-657
Buschhüter, D., Smitka, M., Puschmann, S., Gerber, J. C., Witt, M., Abolmaali, N. D., & Hummel, T. (2008). Correlation between olfactory bulb volume and olfactory function. NeuroImage, 42(2), 498-502. https://doi.org/10.1016/j.neuroimage.2008.05.004
Carmon, J., Heege, J., Necus, J. H., Owen, T. W., Pipa, G., Kaiser, M., Taylor, P. N., & Wang, Y. (2020). Reliability and comparability of human brain structural covariance networks. NeuroImage, 220, 117104. https://doi.org/10.1016/j.neuroimage.2020.117104
Collignon, O., Dormal, G., Albouy, G., Vandewalle, G., Voss, P., Phillips, C., & Lepore, F. (2013). Impact of blindness onset on the functional organization and the connectivity of the occipital cortex. Brain, 136(9), 2769-2783. https://doi.org/10.1093/brain/awt176
Cooper, H. M., Parvopassu, F., Herbin, M., & Magnin, M. (1994). Neuroanatomical pathways linking vision and olfaction in mammals. Psychoneuroendocrinology, 19(5-7), 623-639. https://doi.org/10.1016/0306-4530(94)90046-9
Croy, I., Drechsler, E., Hamilton, P., Hummel, T., & Olausson, H. (2016). Olfactory modulation of affective touch processing-A neurophysiological investigation. NeuroImage, 135, 135-141. https://doi.org/10.1016/j.neuroimage.2016.04.046
Dahnke, R., Ziegler, G., & Gaser, C. (2012). Local adaptive segmentation. HBM. http://dbm.neuro.uni-jena.de/HBM2012/HBM2012-Dahnke02.pdf
De Araujo, I. E., Rolls, E. T., Velazco, M. I., Margot, C., & Cayeux, I. (2005). Cognitive modulation of olfactory processing. Neuron, 46(4), 671-679. https://doi.org/10.1016/j.neuron.2005.04.021
de Villers-Sidani, E., Alzghoul, L., Zhou, X., Simpson, K. L., Lin, R. C., & Merzenich, M. M. (2010). Recovery of functional and structural age-related changes in the rat primary auditory cortex with operant training. Proceedings of the National Academy of Sciences, 107(31), 13900-13905. https://doi.org/10.1073/pnas.1007885107
Delon-Martin, C., Plailly, J., Fonlupt, P., Veyrac, A., & Royet, J. P. (2013). Perfumers' expertise induces structural reorganization in olfactory brain regions. NeuroImage, 68, 55-62. https://doi.org/10.1016/j.neuroimage.2012.11.044
Demattè, M. L., Sanabria, D., & Spence, C. (2009). Olfactory discrimination: When vision matters? Chemical Senses, 34(2), 103-109. https://doi.org/10.1093/chemse/bjn055
Diamond, M. E., Von Heimendahl, M., Knutsen, P. M., Kleinfeld, D., & Ahissar, E. (2008). ‘Where’ and ‘what’ in the whisker sensorimotor system. Nature Reviews Neuroscience, 9(8), 601-612. https://doi.org/10.1038/nrn2411
Ferdenzi, C., Coureaud, G., Camos, V., & Schaal, B. (2010). Attitudes toward everyday odors for children with visual impairments: A pilot study. Journal of Visual Impairment & Blindness, 104(1), 55-59. https://doi.org/10.1177/0145482X1010400109
Fjaeldstad, A., Fernandes, H. M., Van Hartevelt, T. J., Gleesborg, C., Møller, A., Ovesen, T., & Kringelbach, M. L. (2017). Brain fingerprints of olfaction: A novel structural method for assessing olfactory cortical networks in health and disease. Scientific Reports, 7(1), 1-13. https://doi.org/10.1038/srep42534
Fornazieri, M. A., Doty, R. L., Bezerra, T. F. P., de Rezende Pinna, F., Costa, F. O., Voegels, R. L., & Silveira-Moriyama, L. (2019). Relationship of socioeconomic status to olfactory function. Physiology & Behavior, 198, 84-89. https://doi.org/10.1016/j.physbeh.2018.10.011
Frasnelli, J., Collignon, O., Voss, P., & Lepore, F. (2011). Crossmodal plasticity in sensory loss. In A. M. Green, C. E. Chapman, J. F. Kalaska, & F. Lepore (Eds.), Progress in brain research (Vol. 191) (pp. 233-249). Elsevier. https://doi.org/10.1016/B978-0-444-53752-2.00002-3
Frasnelli, J., Lundström, J. N., Boyle, J. A., Djordjevic, J., Zatorre, R. J., & Jones-Gotman, M. (2010). Neuroanatomical correlates of olfactory performance. Experimental Brain Research, 201(1), 1-11. https://doi.org/10.1007/s00221-009-1999-7
Frye, R. E., Schwartz, B. S., & Doty, R. L. (1990). Dose-related effects of cigarette smoking on olfactory function. JAMA, 263(9), 1233-1236. https://doi.org/10.1001/jama.1990.03440090067028
Gellrich, J., Han, P., Manesse, C., Betz, A., Junghanns, A., Raue, C., Schriever, V. A., & Hummel, T. (2018). Brain volume changes in hyposmic patients before and after olfactory training. The Laryngoscope, 128(7), 1531-1536. https://doi.org/10.1002/lary.27045
Gottfried, J. A. (2010). Central mechanisms of odour object perception. Nature Reviews Neuroscience, 11(9), 628-641. https://doi.org/10.1038/nrn2883
Gottfried, J. A., Deichmann, R., Winston, J. S., & Dolan, R. J. (2002). Functional heterogeneity in human olfactory cortex: An event-related functional magnetic resonance imaging study. Journal of Neuroscience, 22(24), 10819-10828. https://doi.org/10.1523/JNEUROSCI.22-24-10819.2002
Gottfried, J. A., & Dolan, R. J. (2003). The nose smells what the eye sees: Crossmodal visual facilitation of human olfactory perception. Neuron, 39(2), 375-386. https://doi.org/10.1016/S0896-6273(03)00392-1
Gudziol, V., Buschhüter, D., Abolmaali, N., Gerber, J., Rombaux, P., & Hummel, T. (2009). Increasing olfactory bulb volume due to treatment of chronic rhinosinusitis-A longitudinal study. Brain, 132(11), 3096-3101. https://doi.org/10.1093/brain/awp243
Haehner, A., Mayer, A. M., Landis, B. N., Pournaras, I., Lill, K., Gudziol, V., & Hummel, T. (2009). High test-retest reliability of the extended version of the “Sniffin' Sticks” test. Chemical Senses, 34(8), 705-711. https://doi.org/10.1093/chemse/bjp057
Haehner, A., Rodewald, A., Gerber, J. C., & Hummel, T. (2008). Correlation of olfactory function with changes in the volume of the human olfactory bulb. Archives of Otolaryngology - Head and Neck Surgery, 134(6), 621-624. https://doi.org/10.1001/archotol.134.6.621
Han, P., Whitcroft, K. L., Fischer, J., Gerber, J., Cuevas, M., Andrews, P., & Hummel, T. (2017). Olfactory brain gray matter volume reduction in patients with chronic rhinosinusitis. International Forum of Allergy & Rhinology, 7(6), 551-556. https://doi.org/10.1002/alr.21922
Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience, 6(11), 877-888. https://doi.org/10.1038/nrn1787
Huart, C., Rombaux, P., & Hummel, T. (2013). Plasticity of the human olfactory system: The olfactory bulb. Molecules, 18(9), 11586-11600. https://doi.org/10.3390/molecules180911586
Hummel, T., Henkel, S., Negoias, S., Galván, J. R., Bogdanov, V., Hopp, P., Hallmeyer-Elgner, S., Gerber, J., Reuner, U., & Haehner, A. (2013). Olfactory bulb volume in patients with temporal lobe epilepsy. Journal of Neurology, 260(4), 1004-1008. https://doi.org/10.1007/s00415-012-6741-x
Hummel, T., Mohammadian, P., & Kobal, G. (1998). Handedness is a determining factor in lateralized olfactory discrimination. Chemical Senses, 23(5), 541-544. https://doi.org/10.1093/chemse/23.5.541
Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). ‘Sniffin' sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22(1), 39-52. https://doi.org/10.1093/chemse/22.1.39
Hummel, T., Urbig, A., Huart, C., Duprez, T., & Rombaux, P. (2015). Volume of olfactory bulb and depth of olfactory sulcus in 378 consecutive patients with olfactory loss. Journal of Neurology, 262(4), 1046-1051. https://doi.org/10.1007/s00415-015-7691-x
Iversen, K. D., Ptito, M., Møller, P., & Kupers, R. (2015). Enhanced chemosensory detection of negative emotions in congenital blindness. Neural Plasticity, 2015, 1-7. https://doi.org/10.1155/2015/469750
Jiang, J., Zhu, W., Shi, F., Liu, Y., Li, J., Qin, W., Li, K., Yu, C., & Jiang, T. (2009). Thick visual cortex in the early blind. Journal of Neuroscience, 29(7), 2205-2211. https://doi.org/10.1523/JNEUROSCI.5451-08.2009
Jones-Gotman, M., & Zatorre, R. J. (1993). Odor recognition memory in humans: Role of right temporal and orbitofrontal regions. Brain and Cognition, 22(2), 182-198. https://doi.org/10.1006/brcg.1993.1033
Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16(8), 1412-1425. https://doi.org/10.1162/0898929042304796
Lane, G., Zhou, G., Noto, T., & Zelano, C. (2020). Assessment of direct knowledge of the human olfactory system. Experimental Neurology, 329, 113304. https://doi.org/10.1016/j.expneurol.2020.113304
Leporé, N., Voss, P., Lepore, F., Chou, Y. Y., Fortin, M., Gougoux, F., Lee, A. D., Brun, C., Lassonde, M., Madsen, S. K., Toga, A. W., & Thompson, P. M. (2010). Brain structure changes visualized in early-and late-onset blind subjects. NeuroImage, 49(1), 134-140. https://doi.org/10.1016/j.neuroimage.2009.07.048
Lötsch, J., Ultsch, A., Eckhardt, M., Huart, C., Rombaux, P., & Hummel, T. (2016). Brain lesion-pattern analysis in patients with olfactory dysfunctions following head trauma. NeuroImage: Clinical, 11, 99-105. https://doi.org/10.1016/j.nicl.2016.01.011
Maller, J. J., Thomson, R. H., Ng, A., Mann, C., Eager, M., Ackland, H., Fitzgerald, P. B., Egan, G., & Rosenfeld, J. V. (2016). Brain morphometry in blind and sighted subjects. Journal of Clinical Neuroscience, 33, 89-95. https://doi.org/10.1016/j.jocn.2016.01.040
Manescu, S., Chouinard-Leclaire, C., Collignon, O., Lepore, F., & Frasnelli, J. (2021). Enhanced odorant localization abilities in congenitally blind but not in late-blind individuals. Chemical Senses, 46, 1-9. https://doi.org/10.1093/chemse/bjaa073
Manescu, S., Poupon, D., Ballester, J., Abdi, H., Valentin, D., Lepore, F., & Frasnelli, J. (2018). Early-blind individuals show impaired performance in wine odor categorization. Neuroscience, 390, 79-87. https://doi.org/10.1016/j.neuroscience.2018.08.012
Mick, G., Cooper, H., & Magnin, M. (1993). Retinal projection to the olfactory tubercle and basal telencephalon in primates. Journal of Comparative Neurology, 327(2), 205-219. https://doi.org/10.1002/cne.903270204
Mishra, J., de Villers-Sidani, E., Merzenich, M., & Gazzaley, A. (2014). Adaptive training diminishes distractibility in aging across species. Neuron, 84(5), 1091-1103. https://doi.org/10.1016/j.neuron.2014.10.034
Mueller, A., Rodewald, A., Reden, J., Gerber, J., von Kummer, R., & Hummel, T. (2005). Reduced olfactory bulb volume in post-traumatic and post-infectious olfactory dysfunction. NeuroReport, 16(5), 475-478. https://doi.org/10.1097/00001756-200504040-00011
Negoias, S., Pietsch, K., & Hummel, T. (2017). Changes in olfactory bulb volume following lateralized olfactory training. Brain Imaging and Behavior, 11(4), 998-1005. https://doi.org/10.1007/s11682-016-9567-9
Nguyen, A. D., Pelavin, P. E., Shenton, M. E., Chilakamarri, P., McCarley, R. W., Nestor, P. G., & Levitt, J. J. (2011). Olfactory sulcal depth and olfactory bulb volume in patients with schizophrenia: An MRI study. Brain Imaging and Behavior, 5(4), 252-261. https://doi.org/10.1007/s11682-011-9129-0
Nguyen, D. T., Rumeau, C., Gallet, P., & Jankowski, R. (2016). Olfactory exploration: State of the art. European Annals of Otorhinolaryngology, Head and Neck Diseases, 133(2), 113-118. https://doi.org/10.1016/j.anorl.2015.08.038
Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). The enigmatic temporal pole: A review of findings on social and emotional processing. Brain, 130(7), 1718-1731. https://doi.org/10.1093/brain/awm052
Öngür, D., & Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex, 10(3), 206-219. https://doi.org/10.1093/cercor/10.3.206
Orhan, K. S., Karabulut, B., Keleş, N., & Değer, K. (2012). Evaluation of factors concerning the olfaction using the Sniffin' Sticks test. Otolaryngology and Head and Neck Surgery, 146(2), 240-246.
Österbauer, R. A., Matthews, P. M., Jenkinson, M., Beckmann, C. F., Hansen, P. C., & Calvert, G. A. (2005). Color of scents: Chromatic stimuli modulate odor responses in the human brain. Journal of Neurophysiology, 93, 3434-3441. https://doi.org/10.1152/jn.00555.2004
Park, H. J., Lee, J. D., Kim, E. Y., Park, B., Oh, M. K., Lee, S., & Kim, J. J. (2009). Morphological alterations in the congenital blind based on the analysis of cortical thickness and surface area. NeuroImage, 47(1), 98-106. https://doi.org/10.1016/j.neuroimage.2009.03.076
Pessoa, L. (2008). On the relationship between emotion and cognition. Nature Reviews Neuroscience, 9(2), 148-158. https://doi.org/10.1038/nrn2317
Prusky, G. T., Harker, K. T., Douglas, R. M., & Whishaw, I. Q. (2002). Variation in visual acuity within pigmented, and between pigmented and albino rat strains. Behavioural Brain Research, 136(2), 339-348. https://doi.org/10.1016/S0166-4328(02)00126-2
Rausch, R., Serafetinides, E. A., & Crandall, P. H. (1977). Olfactory memory in patients with anterior temporal lobectomy. Cortex, 13(4), 445-452. https://doi.org/10.1016/S0010-9452(77)80024-5
Rolls, E. T., & Baylis, L. L. (1994). Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. Journal of Neuroscience, 14(9), 5437-5452. https://doi.org/10.1523/JNEUROSCI.14-09-05437.1994
Rombaux, P., Duprez, T., & Hummel, T. (2009). Olfactory bulb volume in the clinical assessment of olfactory dysfunction. Rhinology, 47(1), 3-9.
Rombaux, P., Huart, C., De Volder, A. G., Cuevas, I., Renier, L., Duprez, T., & Grandin, C. (2010). Increased olfactory bulb volume and olfactory function in early blind subjects. NeuroReport, 21(17), 1069-1073. https://doi.org/10.1097/WNR.0b013e32833fcb8a
Rombaux, P., Mouraux, A., Bertrand, B., Nicolas, G., Duprez, T., & Hummel, T. (2006a). Retronasal and orthonasal olfactory function in relation to olfactory bulb volume in patients with posttraumatic loss of smell. The Laryngoscope, 116(6), 901-905. https://doi.org/10.1097/01.mlg.0000217533.60311.e7
Rombaux, P., Mouraux, A., Bertrand, B., Nicolas, G., Duprez, T., & Hummel, T. (2006b). Olfactory function and olfactory bulb volume in patients with postinfectious olfactory loss. The Laryngoscope, 116(3), 436-439. https://doi.org/10.1097/01.MLG.0000195291.36641.1E
Royet, J. P., Zald, D., Versace, R., Costes, N., Lavenne, F., Koenig, O., & Gervais, R. (2000). Emotional responses to pleasant and unpleasant olfactory, visual, and auditory stimuli: A positron emission tomography study. Journal of Neuroscience, 20(20), 7752-7759. https://doi.org/10.1523/JNEUROSCI.20-20-07752.2000
Schriever, V. A., Reither, N., Gerber, J., Iannilli, E., & Hummel, T. (2013). Olfactory bulb volume in smokers. Experimental Brain Research, 225(2), 153-157. https://doi.org/10.1007/s00221-012-3356-5
Seigneuric, A., Durand, K., Jiang, T., Baudouin, J. Y., & Schaal, B. (2010). The nose tells it to the eyes: Crossmodal associations between olfaction and vision. Perception, 39(11), 1541-1554. https://doi.org/10.1068/p6740
Seo, H. S., Roidl, E., Müller, F., & Negoias, S. (2010). Odors enhance visual attention to congruent objects. Appetite, 54(3), 544-549. https://doi.org/10.1016/j.appet.2010.02.011
Seubert, J., Freiherr, J., Frasnelli, J., Hummel, T., & Lundström, J. N. (2013). Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects. Cerebral Cortex, 23(10), 2448-2456. https://doi.org/10.1093/cercor/bhs230
Simon, H. J., Divenyi, P. L., & Lotze, A. (2002). Lateralization of narrow-band noise by blind and sighted listeners. Perception, 31(7), 855-873. https://doi.org/10.1068/p3338
Smeets, M. A., Schifferstein, H. N., Boelema, S. R., & Lensvelt-Mulders, G. (2008). The odor awareness scale: A new scale for measuring positive and negative odor awareness. Chemical Senses, 33(8), 725-734. https://doi.org/10.1093/chemse/bjn038
Sorokowska, A., Sorokowski, P., Karwowski, M., Larsson, M., & Hummel, T. (2019). Olfactory perception and blindness: A systematic review and meta-analysis. Psychological Research, 83(8), 1595-1611. https://doi.org/10.1007/s00426-018-1035-2
Stevenson, R. J. (2010). An initial evaluation of the functions of human olfaction. Chemical Senses, 35(1), 3-20. https://doi.org/10.1093/chemse/bjp083
Thomann, P. A., Dos Santos, V., Toro, P., Schönknecht, P., Essig, M., & Schröder, J. (2009). Reduced olfactory bulb and tract volume in early Alzheimer's disease-A MRI study. Neurobiology of Aging, 30(5), 838-841. https://doi.org/10.1016/j.neurobiolaging.2007.08.001
Touj, S., Cloutier, S., Jemâa, A., Piché, M., Bronchti, G., & Al Aïn, S. (2020). Better olfactory performance and larger olfactory bulbs in a mouse model of congenital blindness. Chemical Senses, 45(7), 523-531. https://doi.org/10.1093/chemse/bjaa052
Turetsky, B. I., Moberg, P. J., Yousem, D. M., Doty, R. L., Arnold, S. E., & Gur, R. E. (2000). Reduced olfactory bulb volume in patients with schizophrenia. American Journal of Psychiatry, 157(5), 828-830. https://doi.org/10.1176/appi.ajp.157.5.828
Uchida, N., & Mainen, Z. F. (2003). Speed and accuracy of olfactory discrimination in the rat. Nature Neuroscience, 6(11), 1224-1229. https://doi.org/10.1038/nn1142
von Heimendahl, M., Itskov, P. M., Arabzadeh, E., & Diamond, M. E. (2007). Neuronal activity in rat barrel cortex underlying texture discrimination. PLoS Biology, 5(11), e305. https://doi.org/10.1371/journal.pbio.0050305
Voss, P., Collignon, O., Lassonde, M., & Lepore, F. (2010). Adaptation to sensory loss. Wiley Interdisciplinary Reviews: Cognitive Science, 1(3), 308-328. https://doi.org/10.1002/wcs.13
Voss, P., Thomas, M. E., Cisneros-Franco, J. M., & de Villers-Sidani, É. (2017). Dynamic brains and the changing rules of neuroplasticity: Implications for learning and recovery. Frontiers in Psychology, 8, 1657. https://doi.org/10.3389/fpsyg.2017.01657
Whitcroft, K. L., Cuevas, M., Andrews, P., & Hummel, T. (2018). Monitoring olfactory function in chronic rhinosinusitis and the effect of disease duration on outcome. International Forum of Allergy & Rhinology, 8(7), 769-776. https://doi.org/10.1002/alr.22104
Yao, L., Pinto, J. M., Yi, X., Li, L., Peng, P., & Wei, Y. (2014). Gray matter volume reduction of olfactory cortices in patients with idiopathic olfactory loss. Chemical Senses, 39(9), 755-760. https://doi.org/10.1093/chemse/bju047
Yousem, D. M., Geckle, R. J., Bilker, W. B., Kroger, H., & Doty, R. L. (1999). Posttraumatic smell loss: Relationship of psychophysica tests and volumes of the olfactory bulbs and tracts and the temporal lobes. Academic Radiology, 6(5), 264-272. https://doi.org/10.1016/S1076-6332(99)80449-8
Yousem, D. M., Geckle, R. J., Bilker, W. B., McKeown, D. A., & Doty, R. L. (1996). Posttraumatic olfactory dysfunction: MR and clinical evaluation. American Journal of Neuroradiology, 17(6), 1171-1179.
Yousem, D. M., Williams, S. C., Howard, R. O., Andrew, C., Simmons, A., Allin, M., Geckle, R. J., Suskind, D., Bullmore, E. T., Brammer, M. J., & Doty, R. L. (1997). Functional MR imaging during odor stimulation: Preliminary data. Radiology, 204(3), 833-838. https://doi.org/10.1148/radiology.204.3.9280268
Yousry, I., Camelio, S., Schmid, U. D., Horsfield, M. A., Wiesmann, M., Brückmann, H., & Yousry, T. A. (2000). Visualization of cranial nerves I-XII: value of 3D CISS and T2-weighted FSE sequences. European Radiology, 10(7), 1061-1067. https://doi.org/10.1007/s003300000452
Zatorre, R. J., & Jones-Gotman, M. (1990). Right-nostril advantage for discrimination of odors. Perception & Psychophysics, 47(6), 526-531. https://doi.org/10.3758/BF03203105
Zhou, W., Jiang, Y., He, S., & Chen, D. (2010). Olfaction modulates visual perception in binocular rivalry. Current Biology, 20(15), 1356-1358. https://doi.org/10.1016/j.cub.2010.05.059
Zou, L. Q., van Hartevelt, T. J., Kringelbach, M. L., Cheung, E. F., & Chan, R. C. (2016). The neural mechanism of hedonic processing and judgment of pleasant odors: An activation likelihood estimation meta-analysis. Neuropsychology, 30(8), 970-979. https://doi.org/10.1037/neu0000292