Distinct representations of olfactory information in different cortical centres
Open accessAbstract
Sensory information is transmitted to the brain where it must be processed to translate stimulus features into appropriate behavioural output. In the olfactory system, distributed neural activity in the nose is converted into a segregated map in the olfactory bulb. Here we investigate how this ordered representation is transformed in higher olfactory centres in mice. We have developed a tracing strategy to define the neural circuits that convey information from individual glomeruli in the olfactory bulb to the piriform cortex and the cortical amygdala. The spatial order in the bulb is discarded in the piriform cortex; axons from individual glomeruli project diffusely to the piriform without apparent spatial preference. In the cortical amygdala, we observe broad patches of projections that are spatially stereotyped for individual glomeruli. These projections to the amygdala are overlapping and afford the opportunity for spatially localized integration of information from multiple glomeruli. The identification of a distributive pattern of projections to the piriform and stereotyped projections to the amygdala provides an anatomical context for the generation of learned and innate behaviours.
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Outputs to the amygdala via the olfactory bulbs or transport through brain extracellular fluid from olfactory bulb and brainstem delivery sites after intranasal delivery may facilitate reductions in amygdala activity via a local GABAergic circuit.
“Outputs to the amygdala via the olfactory bulbs (Sosulski et al., 2012) or transport through brain extracellular fluid (Neumann et al., 2013) from olfactory bulb and brainstem delivery sites after intranasal delivery may facilitate these reduc-tions in amygdala activity via a local GABAergic circuit.”
From Low dose intranasal oxytocin delivered with Breath Powered device dampens amygdala response to emotional stimuli: A peripheral effect-controlled within-subjects randomized dose-response fMRI trial (2016) · cites this paper as Sosulski et al., 2012
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Cites
A novel multigene family may encode odorant receptors: A molecular basis for odor recognition
Buck, L., & Axel, R. (1991) · Cell · doi:10.1016/0092-8674(91)90418-x · Cited by 4,987 · see citing works
Self-citationCombinatorial Receptor Codes for Odors
Malnic, B., Hirono, J., Sato, T., & Buck, L. B. (1999) · Cell · doi:10.1016/s0092-8674(00)80581-4 · Cited by 2,302 · see citing works
Visualizing an Olfactory Sensory Map
Mombaerts, P., Wang, F., Dulac, C. G., Chao, S. K., Nemes, A., Mendelsohn, M. M., Edmondson, J., & Axel, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81387-2 · Cited by 1,992 · see citing works
Self-citationTopographic organization of sensory projections to the olfactory bulb
Vassar, R. J., Chao, S. K., Sitcheran, R., ̃ez, J. M. N., Vosshall, L. B., & Axel, R. (1994) · Cell · doi:10.1016/0092-8674(94)90029-9 · Cited by 1,281 · see citing works
Self-citationRessler, K. J., Sullivan, S. L., & Buck, L. B. (1994) · Cell · doi:10.1016/0092-8674(94)90015-9 · Cited by 1,202 · see citing works
Allelic inactivation regulates olfactory receptor gene expression
Chess, A. J., Simon, I., Cedar, H., & Axel, R. (1994) · Cell · doi:10.1016/s0092-8674(94)90562-2 · Cited by 1,066 · see citing works
Self-citationMolecular Architecture of Smell and Taste in Drosophila
Vosshall, L. B., & Stocker, R. F. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094306 · Cited by 860 · see citing works
Innate and conditioned reactions to threat in rats with amygdaloid lesions.
Blanchard, D. C., & Blanchard, R. J. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033521 · Cited by 753 · see citing works
de Olmos, J. S., Hardy, H., & Heimer, L. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901810202 · Cited by 712 · see citing works
Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb
Rubin, B. D., & Katz, L. C. (1999) · Neuron · doi:10.1016/s0896-6273(00)80803-x · Cited by 669 · see citing works
Representations of Odor in the Piriform Cortex
Stettler, D. D., & Axel, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.005 · Cited by 583 · see citing works
Self-citationCortical representations of olfactory input by trans-synaptic tracing
Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I. R., Wall, N. R., Taniguchi, H., Tasic, B., Huang, Z. J., He, Z., et al. (2010) · Nature · doi:10.1038/nature09714 · Cited by 546 · see citing works
Price, J. L. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901500105 · Cited by 530 · see citing works
Odor Representations in Olfactory Cortex: “Sparse” Coding, Global Inhibition, and Oscillations
Poo, C., & Isaacson, J. S. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.022 · Cited by 469 · see citing works
The Drosophila pheromone cVA activates a sexually dimorphic neural circuit
Datta, S. R., Vasconcelos, M. L., Ruta, V., Luo, S. X., Wong, A. M., Demir, E., Flores, J., Balonze, K., Dickson, B. J., & Axel, R. (2008) · Nature · doi:10.1038/nature06808 · Cited by 383 · see citing works
Self-citationBozza, T. C., McGann, J. P., Mombaerts, P., et al. (2004) · Neuron · doi:10.1016/s0896-6273(04)00144-8 · Cited by 360 · see citing works
The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat
Haberly, L. B., & Price, J. L. (1977) · Brain Research · doi:10.1016/0006-8993(77)90978-7 · Cited by 342 · see citing works
Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons
Ghosh, S. D., Larson, S., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., & Baldwin, K. K. (2011) · Nature · doi:10.1038/nature09945 · Cited by 291 · see citing works
Self-citationGene Switching and the Stability of Odorant Receptor Gene Choice
Shykind, B., Rohani, S., O'Donnell, S., Nemes, A., Mendelsohn, M. M., Sun, Y., Axel, R., & Barnea, G. (2004) · Cell · doi:10.1016/j.cell.2004.05.015 · Cited by 273 · see citing works
Self-citationScott, J. W., McBride, R. L., & Schneider, S. P. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901940304 · Cited by 234 · see citing works
Targeting genes for self-excision in the germ linePreprint
Bunting, M., Bernstein, K. E., Greer, J. M., Capecchi, M. R., & Thomas, K. R. (1999) · Genes & Development · doi:10.1101/gad.13.12.1524 · Cited by 234 · see citing works
Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex
Rennaker, R. L., Chen, C.-F. F., Ruyle, A. M., Sloan, A. M., & Wilson, D. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4072-06.2007 · Cited by 198 · see citing works
Efferent projections of the main and the accessory olfactory bulb in the tree shrew (Tupaia glis)
Skeen, L. C., & Hall, W. C. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901720102 · Cited by 143 · see citing works
XuvTools: free, fast and reliable stitching of large 3D datasets
Emmenlauer, M., Ronneberger, O., Ponti, A., Schwarb, P., Griffa, A., Filippi, A., Nitschke, R., Driever, W., & BURKHARDT, H. (2009) · Journal of Microscopy · doi:10.1111/j.1365-2818.2008.03094.x · Cited by 142 · see citing works
Ojima, H., Mori, K., & Kishi, K. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902300107 · Cited by 131 · see citing works
Luskin, M. B., & Price, J. L. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902090304 · Cited by 116 · see citing works
Scott, J. W. (1981) · Journal of Neurophysiology · doi:10.1152/jn.1981.46.5.918 · Cited by 110 · see citing works
Schneider, S. P., & Scott, J. W. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.50.2.358 · Cited by 102 · see citing works
Odor representations in olfactory cortex
Poo, C. (2010) · eScholarship (California Digital Library) · Cited by 101 · see citing works
Evolutionary changes of the number of olfactory receptor genes in the human and mouse lineages
Niimura, Y., & Nei, M. (2005) · Gene · doi:10.1016/j.gene.2004.09.027 · Cited by 67 · see citing works
Buonviso, N., Revial, M. F., & Jourdan, F. (1991) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1991.tb00836.x · Cited by 55 · see citing works
Olfactory discrimination in rats with anterior amygdala lesions.
Slotnick, B. M. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.5.956 · Cited by 37 · see citing works
Olfactory discrimination in rats with anterior amygdala lesions.
Slotnick, B. M. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.5.956 · Cited by 29 · see citing works
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The importance of mixed selectivity in complex cognitive tasks
Rigotti, M., Barak, O., Warden, M. R., Wang, X.-J., Daw, N. D., Miller, E. K., & Fusi, S. (2013) · Nature · doi:10.1038/nature12160 · Cited by 1,639 · see citing works
Rethinking the Emotional Brain
LeDoux, J. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.004 · Cited by 1,594 · see citing works
“…processing, for which analogies in behaviorally relevant peripheral odor-encoding and central representation occur using similar organizational principles in anatomically distinct (nonhomologous) structures in Drosophila and rodents (see Bargmann, 2006; Sosulski et al., 2011; Wang et al., 2011).”
At the interface of sensory and motor dysfunctions and Alzheimer’s disease.
Albers, M. W., Gilmore, G. C., Kaye, J., Murphy, C., Wingfield, A., Bennett, D. A., Boxer, A. L., Buchman, A. S., Cruickshanks, K. J., Devanand, D. P., et al. (2015) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2014.04.514 · Cited by 589 · see citing works
The connectome of an insect brain
Winding, M., Pedigo, B. D., Barnes, C. L., Patsolic, H. G., Park, Y., Kazimiers, T., Fushiki, A., Andrade, I. V., Khandelwal, A., Valdes-Aleman, J., et al. (2023) · Science · doi:10.1126/science.add9330 · Cited by 435 · see citing works
Oxytocin enhances social recognition by modulating cortical control of early olfactory processing
Oettl, L.-L., Ravi, N., Schneider, M., Scheller, M. F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R. C., Chao, M. V., Young, W. S., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.033 · Cited by 359 · see citing works
Dendritic spines and distributed circuits
Yuste, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.024 · Cited by 298 · see citing works
Sex-specific processing of social cues in the medial amygdala
Bergan, J. F., Ben-Shaul, Y., & Dulac, C. (2014) · eLife · doi:10.7554/elife.02743 · Cited by 237 · see citing works
The wiring diagram of a glomerular olfactory system
Berck, M. E., Khandelwal, A., Claus, L., Hernandez-Nunez, L., Si, G., Tabone, C. J., Li, F., Truman, J. W., Fetter, R. D., Louis, M., et al. (2016) · eLife · doi:10.7554/elife.14859 · Cited by 209 · see citing works
From chemotaxis to the cognitive map: The function of olfaction
Jacobs, L. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201880109 · Cited by 227 · see citing works
Social transmission and buffering of synaptic changes after stress
Sterley, T.-L., Baimoukhametova, D., Füzesi, T., Zurek, A. A., Daviu, N., Rasiah, N. P., Rosenegger, D., & Bains, J. S. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0044-6 · Cited by 179 · see citing works
Intranasal administration of oxytocin: behavioral and clinical effects, a review
Veening, J. G., & Olivier, B. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.04.012 · Cited by 169 · see citing works
Dolan, M.-J., Frechter, S., Bates, A. S., Dan, C., Huoviala, P., Roberts, R. J., Schlegel, P., Dhawan, S., Tabano, R., Dionne, H., et al. (2019) · eLife · doi:10.7554/elife.43079 · Cited by 169 · see citing works
Feinberg, T. E., & Mallatt, J. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00667 · Cited by 158 · see citing works
Quintana, D. S., Alvares, G. A., Hickie, I. B., & Guastella, A. J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.011 · Cited by 149 · see citing works
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Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence
Choe, H. K., Reed, M. D., Benavidez, N., Montgomery, D., Soares, N., Yim, Y. S., & Choi, G. B. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.022 · Cited by 124 · see citing works
Functional and anatomical specificity in a higher olfactory centre
Frechter, S., Bates, A. S., Tootoonian, S., Dolan, M.-J., Manton, J., Jamasb, A. R., Kohl, J., Bock, D., & Jefferis, G. (2019) · eLife · doi:10.7554/elife.44590 · Cited by 105 · see citing works
Quintana, D. S., Westlye, L. T., Alnæs, D., Rustan, Ø. G., Kaufmann, T., Smerud, K. T., Mahmoud, R. A., Djupesland, P. G., & Andreassen, O. A. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.04.010 · Cited by 102 · see citing works
Interneurons, tau and amyloid-β in the piriform cortex in Alzheimer’s disease
Saiz-Sanchez, D., De la Rosa-Prieto, C., Ubeda-Banon, I., & Martinez-Marcos, A. (2015) · Brain Structure and Function · doi:10.1007/s00429-014-0771-3 · Cited by 79 · see citing works
Carvalho, V. M. A., Nakahara, T. S., Cardozo, L. M., Souza, M. A. A., Camargo, A. P., Trintinalia, G. Z., Ferraz, E., & Papes, F. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00283 · Cited by 25 · see citing works
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- Authors
- Sosulski, D. L., Bloom, M. L., Cutforth, T., Axel, R., & Datta, S. R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Axel, Richard
- Venue
- Nature
- Published
- 2011-03-30
- Volume
- 472
- Issue
- 7342
- Pages
- 213-216
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3354569
- OpenAlex
- W2084642506
- Cited by
- 479
- References
- 33
- Citations by year
- 2026: 21 · 2025: 26 · 2024: 29 · 2023: 22 · 2022: 25 · 2021: 33 · 2020: 39 · 2019: 27 · 2018: 29 · 2017: 32 · 2016: 45 · 2015: 29 · 2014: 41 · 2013: 27 · 2012: 34
- FWCI
- 20.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (1dp2od007109-01)
- National Institute on Deafness and Other Communication Disorders (R01DC011558)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007430)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- olfactory processing, olfactory bulb, glomeruli, piriform cortex, cortical amygdala
- MeSH terms
- Amygdala, Animals, Axons, Brain Mapping, Olfactory Bulb, Olfactory Pathways, Mice, Olfactory Perception, Neuroanatomical Tract-Tracing Techniques
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