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How the sense of smell influences cognition throughout life

  • Johanna K. Kostka

    Johanna K. Kostka is currently completing her Ph.D. at the Institute of Developmental Neurophysiology at the Center of Molecular Neurobiology in Hamburg-Eppendorf. She received her bachelor’s degree in Biophysics at the Humboldt University of Berlin and her master’s degree in Brain and Cognitive Science at the University of Amsterdam. Her research focuses on the role of olfactory processing for the development of cortical and hippocampal networks. She is using in vivo extracellular electrophysiology as well as opto- and chemogenetics to investigate network interactions between the olfactory bulb and brain areas, such as the entorhinal cortex, the hippocampus, and the prefrontal cortex.

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    und Sebastian H. Bitzenhofer

    Sebastian H. Bitzenhofer is a Junior Research Group Leader associated with the Institute of Developmental Neurophysiology at the University Medical Center Hamburg-Eppendorf. He received his Dr. rer. nat. at the University of Hamburg in 2017, before he did a postdoc at the Center for Neural Circuits and Behavior at the University of California San Diego. He uses a mix of electrophysiological and optogenetic approaches to study neural circuits and population dynamics in mice. In 2021, he was awarded with the Bernard Katz Lecture for his work on the development of the prefrontal cortex.

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Veröffentlicht/Copyright: 6. Juni 2022
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Aus der Zeitschrift Neuroforum Band 28 Heft 3

Abstract

Although mostly unaware, we constantly navigate a complex landscape of airborne molecules. The perception of these molecules helps us navigate, shapes our social life, and can trigger emotionally charged memories transporting us back to the past within a split second. While the processing of olfactory information in early sensory areas is well understood, how the sense of smell affects cognition only recently gained attention in the field of neuroscience. Here, we review links between olfaction and cognition and explore the idea that the activity in olfactory areas may be critical for coordinating cognitive networks. Further, we discuss how olfactory activity may shape the development of cognitive networks and associations between the decline of olfactory and cognitive abilities in aging. Olfaction provides a great tool to study large-scale networks underlying cognitive abilities and bears the potential for a better understanding of cognitive symptoms associated with many mental disorders.

Zusammenfassung

Obwohl meist nicht bewusst, navigieren wir ständig durch eine komplexe Landschaft von Duftstoffen. Die Wahrnehmung dieser Duftstoffe hilft uns bei der Orientierung, prägt unser soziales Leben und kann emotionale Erinnerungen auslösen, die uns innerhalb von Sekundenbruchteilen in die Vergangenheit zurückversetzen. Während die Verarbeitung olfaktorischer Informationen in frühen sensorischen Arealen gut verstanden ist, ist die Frage wie der Geruchssinn die Kognition beeinflusst erst vor kurzem in das Blickfeld der neurowissenschaftlichen Forschung gerückt. Wir diskutieren hier das Zusammenspiel zwischen Geruchssinn und Kognition und untersuchen die Idee, dass die Aktivität in olfaktorischen Arealen entscheidend zur Koordination kognitiver Netzwerkaktivität beiträgt. Darüber hinaus diskutieren wir, wie olfaktorische Aktivität die Entwicklung kognitiver Netzwerke beeinflussen kann, sowie Assoziationen zwischen dem Rückgang olfaktorischer und kognitiver Fähigkeiten im Alter. Der Geruchssinn bietet ein großartiges Werkzeug zur Untersuchung weitläufiger Netzwerke, die kognitiven Fähigkeiten zugrunde liegen, und birgt das Potenzial für ein besseres Verständnis kognitiver Symptome, die mit vielen psychischen Störungen einhergehen.


Corresponding author: Johanna K. Kostka, Center for Molecular Neurobiology Hamburg, Institute of Developmental Neurophysiology, University Medical Center Hamburg-Eppendorf, 20251, Hamburg, Germany, E-mail: ; and Sebastian H. Bitzenhofer, Center for Molecular Neurobiology Hamburg, Institute of Developmental Neurophysiology, University Medical Center Hamburg-Eppendorf, Falkenried 94, 20251, Hamburg, Germany, E-mail:

Award Identifier / Grant number: 178316478 - B5

Award Identifier / Grant number: Ha4466/11-1

Award Identifier / Grant number: ERC-2015-CoG 681577

About the authors

Johanna K. Kostka

Johanna K. Kostka is currently completing her Ph.D. at the Institute of Developmental Neurophysiology at the Center of Molecular Neurobiology in Hamburg-Eppendorf. She received her bachelor’s degree in Biophysics at the Humboldt University of Berlin and her master’s degree in Brain and Cognitive Science at the University of Amsterdam. Her research focuses on the role of olfactory processing for the development of cortical and hippocampal networks. She is using in vivo extracellular electrophysiology as well as opto- and chemogenetics to investigate network interactions between the olfactory bulb and brain areas, such as the entorhinal cortex, the hippocampus, and the prefrontal cortex.

Sebastian H. Bitzenhofer

Sebastian H. Bitzenhofer is a Junior Research Group Leader associated with the Institute of Developmental Neurophysiology at the University Medical Center Hamburg-Eppendorf. He received his Dr. rer. nat. at the University of Hamburg in 2017, before he did a postdoc at the Center for Neural Circuits and Behavior at the University of California San Diego. He uses a mix of electrophysiological and optogenetic approaches to study neural circuits and population dynamics in mice. In 2021, he was awarded with the Bernard Katz Lecture for his work on the development of the prefrontal cortex.

Acknowledgments

We thank Dr. Ileana L. Hanganu-Opatz for feedback to the present manuscript and financial support.

  1. Author contributions: Both authors equally contributed to the manuscript.

  2. Research funding: This work was supported by grants of the European Research Council (ERC-2015-CoG 681577 to Prof. Dr. Ileana L. Hanganu-Opatz) and the German Research Foundation (Ha4466/11-1 and 178316478 - B5 to Prof. Dr. Ileana L. Hanganu-Opatz).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Ackels, T., Jordan, R., Schaefer, A.T., and Fukunaga, I. (2020). Respiration-locking of olfactory receptor and projection neurons in the mouse olfactory bulb and its modulation by brain state. Front. Cell. Neurosci. 14, 1662–5102, doi:https://doi.org/10.3389/fncel.2020.00220.Suche in Google Scholar PubMed PubMed Central

Armstrong, C.M., DeVito, L.M., and Cleland, T.A. (2006). One-trial associative odor learning in neonatal mice. Chem. Senses 31, 343–349. https://doi.org/10.1093/chemse/bjj038.Suche in Google Scholar PubMed

Arshamian, A., Iravani, B., Majid, A., and Lundström, J.N. (2018). Respiration modulates olfactory memory consolidation in humans. J. Neurosci. 38, 10286–10294. https://doi.org/10.1523/JNEUROSCI.3360-17.2018.Suche in Google Scholar PubMed PubMed Central

Attems, J., Walker, L., and Jellinger, K.A. (2015). Olfaction and aging: a mini-review. GER 61, 485–490. https://doi.org/10.1159/000381619.Suche in Google Scholar PubMed

Batista-Brito, R., Close, J., Machold, R., and Fishell, G. (2008). The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 28, 3966–3975. https://doi.org/10.1523/JNEUROSCI.5625-07.2008.Suche in Google Scholar PubMed PubMed Central

Biskamp, J., Bartos, M., and Sauer, J.-F. (2017). Organization of prefrontal network activity by respiration-related oscillations. Sci. Rep. 7, 45508. https://doi.org/10.1038/srep45508.Suche in Google Scholar PubMed PubMed Central

Bitzenhofer, S.H., Pöpplau, J.A., Chini, M., Marquardt, A., and Hanganu-Opatz, I.L. (2021). A transient developmental increase in prefrontal activity alters network maturation and causes cognitive dysfunction in adult mice. Neuron 109, 1350–1364.e6 https://doi.org/10.1016/j.neuron.2021.02.011.Suche in Google Scholar PubMed PubMed Central

Bitzenhofer, S.H., Westeinde, E.A., Zhang, H.-X.B., and Isaacson, J.S. (2022). Rapid odor processing by layer 2 subcircuits in lateral entorhinal cortex. Elife 11, e75065. https://doi.org/10.7554/eLife.75065.Suche in Google Scholar PubMed PubMed Central

Boyd, A.M., Sturgill, J.F., Poo, C., and Isaacson, J.S. (2012). Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161–1174. https://doi.org/10.1016/j.neuron.2012.10.020.Suche in Google Scholar PubMed PubMed Central

Cecchini, M.P., Federico, A., Zanini, A., Mantovani, E., Masala, C., Tinazzi, M., and Tamburin, S. (2019). Olfaction and taste in Parkinson’s disease: the association with mild cognitive impairment and the single cognitive domain dysfunction. J. Neural. Transm. 126, 585–595. https://doi.org/10.1007/s00702-019-01996-z.Suche in Google Scholar PubMed

Chen, Z., and Padmanabhan, K. (2022). Top-down feedback enables flexible coding strategies in the olfactory cortex. Cell Rep. 38, 110545. https://doi.org/10.1016/j.celrep.2022.110545.Suche in Google Scholar PubMed

Chini, M., Pöpplau, J.A., Lindemann, C., Carol-Perdiguer, L., Hnida, M., Oberländer, V., Xu, X., Ahlbeck, J., Bitzenhofer, S.H., Mulert, C., et al.. (2020). Resolving and rescuing developmental miswiring in a mouse model of cognitive impairment. Neuron 105, 60–74.e7 https://doi.org/10.1016/j.neuron.2019.09.042.Suche in Google Scholar PubMed PubMed Central

Doty, R.L. (2012). Olfaction in Parkinson’s disease and related disorders. Neurobiol. Dis. 46, 527–552. https://doi.org/10.1016/j.nbd.2011.10.026.Suche in Google Scholar PubMed PubMed Central

Douaud, G., Lee, S., Alfaro-Almagro, F., Arthofer, C., Wang, C., McCarthy, P., Lange, F., Andersson, J.L.R., Griffanti, L., Duff, E., et al.. (2022). SARS-CoV-2 is associated with changes in brain structure in UK Biobank. Nature 604, 697–707. https://doi.org/10.1038/s41586-022-04569-5.Suche in Google Scholar PubMed PubMed Central

Fischler-Ruiz, W., Clark, D.G., Joshi, N.R., Devi-Chou, V., Kitch, L., Schnitzer, M., Abbott, L.F., and Axel, R. (2021). Olfactory landmarks and path integration converge to form a cognitive spatial map. Neuron 109, 4036–4049.e5 https://doi.org/10.1016/j.neuron.2021.09.055.Suche in Google Scholar PubMed

Fletcher, M.L., Smith, A.M., Best, A.R., and Wilson, D.A. (2005). High-frequency oscillations are not necessary for simple olfactory discriminations in young rats. J. Neurosci. 25, 792–798. https://doi.org/10.1523/JNEUROSCI.4673-04.2005.Suche in Google Scholar PubMed PubMed Central

Gourévitch, B., Kay, L.M., and Martin, C. (2010). Directional coupling from the olfactory bulb to the Hippocampus during a Go/No-Go odor discrimination task. J. Neurophysiol. 103, 2633–2641. https://doi.org/10.1152/jn.01075.2009.Suche in Google Scholar PubMed PubMed Central

Grady, C.L., Furey, M.L., Pietrini, P., Horwitz, B., and Rapoport, S.I. (2001). Altered brain functional connectivity and impaired short-term memory in Alzheimer’s disease. Brain 124, 739–756. https://doi.org/10.1093/brain/124.4.739.Suche in Google Scholar PubMed

Gretenkord, S., Kostka, J.K., Hartung, H., Watznauer, K., Fleck, D., Minier-Toribio, A., Spehr, M., and Hanganu-Opatz, I.L. (2019). Coordinated electrical activity in the olfactory bulb gates the oscillatory entrainment of entorhinal networks in neonatal mice. PLoS Biol. 17, e2006994. https://doi.org/10.1371/journal.pbio.2006994.Suche in Google Scholar PubMed PubMed Central

Hartung, H., Brockmann, M.D., Pöschel, B., Feo, V.D., and Hanganu-Opatz, I.L. (2016). Thalamic and entorhinal network activity differently modulates the functional development of prefrontal–hippocampal interactions. J. Neurosci. 36, 3676–3690. https://doi.org/10.1523/JNEUROSCI.3232-15.2016.Suche in Google Scholar PubMed PubMed Central

Heck, D.H., Kozma, R., and Kay, L.M. (2019). The rhythm of memory: how breathing shapes memory function. J. Neurophysiol. 122, 563–571. https://doi.org/10.1152/jn.00200.2019.Suche in Google Scholar PubMed PubMed Central

Hirata, T., Shioi, G., Abe, T., Kiyonari, H., Kato, S., Kobayashi, K., Mori, K., and Kawasaki, T. (2019). A novel birthdate-labeling method reveals segregated parallel projections of mitral and external tufted cells in the main olfactory system. ENeuro 6, ENEURO.0234-19.2019. https://doi.org/10.1523/ENEURO.0234-19.2019.Suche in Google Scholar PubMed PubMed Central

Huang, G.-D., Jiang, L.-X., Su, F., Wang, H.-L., Zhang, C., and Yu, X. (2020). A novel paradigm for assessing olfactory working memory capacity in mice. Transl. Psychiatry 10, 1–16. https://doi.org/10.1038/s41398-020-01120-w.Suche in Google Scholar PubMed PubMed Central

Igarashi, K.M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W.R., et al.. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970–7985. https://doi.org/10.1523/JNEUROSCI.0154-12.2012.Suche in Google Scholar PubMed PubMed Central

Igarashi, K.M., Lu, L., Colgin, L.L., Moser, M.-B., and Moser, E.I. (2014). Coordination of entorhinal–hippocampal ensemble activity during associative learning. Nature 510, 143–147. https://doi.org/10.1038/nature13162.Suche in Google Scholar PubMed

Karalis, N., and Sirota, A. (2022). Breathing coordinates cortico-hippocampal dynamics in mice during offline states. Nat. Commun. 13, 467. https://doi.org/10.1038/s41467-022-28090-5.Suche in Google Scholar PubMed PubMed Central

Kay, L.M., Beshel, J., Brea, J., Martin, C., Rojas-Líbano, D., and Kopell, N. (2009). Olfactory oscillations: the what, how and what for. Trends Neurosci. 32, 207–214. https://doi.org/10.1016/j.tins.2008.11.008.Suche in Google Scholar PubMed PubMed Central

Khan, U.A., Liu, L., Provenzano, F.A., Berman, D.E., Profaci, C.P., Sloan, R., Mayeux, R., Duff, K.E., and Small, S.A. (2014). Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer’s disease. Nat. Neurosci. 17, 304–311. https://doi.org/10.1038/nn.3606.Suche in Google Scholar PubMed PubMed Central

Kostka, J.K., and Bitzenhofer, S.H. (2022). Postnatal development of centrifugal inputs to the olfactory bulb. Front. Neurosci. 16. https://doi.org/10.3389/fnins.2022.815282.Suche in Google Scholar PubMed PubMed Central

Kostka, J.K., and Hanganu-Opatz, I.L. (2021). Olfactory-driven beta band entrainment of limbic circuitry during neonatal development, BioRxiv 2021.10.04.463041. https://doi.org/10.1101/2021.10.04.463041v2.Suche in Google Scholar

Leitner, F.C., Melzer, S., Lütcke, H., Pinna, R., Seeburg, P.H., Helmchen, F., and Monyer, H. (2016). Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nat. Neurosci. 19, 935–944. https://doi.org/10.1038/nn.4303.Suche in Google Scholar PubMed

Li, Y., Xu, J., Liu, Y., Zhu, J., Liu, N., Zeng, W., Huang, N., Rasch, M.J., Jiang, H., Gu, X., et al.. (2017). A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning. Nat. Neurosci. 20, 559–570. https://doi.org/10.1038/nn.4517.Suche in Google Scholar PubMed

Lockmann, A.L.V., Laplagne, D.A., and Tort, A.B.L. (2018). Olfactory bulb drives respiration-coupled beta oscillations in the rat hippocampus. Eur. J. Neurosci. 48, 2663–2673. https://doi.org/10.1111/ejn.13665.Suche in Google Scholar PubMed

Logan, D.W., Brunet, L.J., Webb, W.R., Cutforth, T., Ngai, J., and Stowers, L. (2012). Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr. Biol. 22, 1998–2007. https://doi.org/10.1016/j.cub.2012.08.041.Suche in Google Scholar PubMed PubMed Central

Lopez-Rojas, J., de Solis, C.A., Leroy, F., Kandel, E.R., and Siegelbaum, S.A. (2022). A direct lateral entorhinal cortex to hippocampal CA2 circuit conveys social information required for social memory. Neuron 110, 1559–1572.e4, doi:https://doi.org/10.1016/j.neuron.2022.01.028.Suche in Google Scholar PubMed PubMed Central

Luo, W., Yun, D., Hu, Y., Tian, M., Yang, J., Xu, Y., Tang, Y., Zhan, Y., Xie, H., and Guan, J.-S. (2022). Acquiring new memories in neocortex of hippocampal-lesioned mice. Nat. Commun. 13, 1601. https://doi.org/10.1038/s41467-022-29208-5.Suche in Google Scholar PubMed PubMed Central

Martini, F.J., Guillamón-Vivancos, T., Moreno-Juan, V., Valdeolmillos, M., and López-Bendito, G. (2021). Spontaneous activity in developing thalamic and cortical sensory networks. Neuron 109, 2519–2534, doi:https://doi.org/10.1016/j.neuron.2021.06.026.Suche in Google Scholar PubMed PubMed Central

Mori, K., Manabe, H., Narikiyo, K., and Onisawa, N. (2013). Olfactory consciousness and gamma oscillation couplings across the olfactory bulb, olfactory cortex, and orbitofrontal cortex. Front. Psychol. 4. https://doi.org/10.3389/fpsyg.2013.00743.Suche in Google Scholar PubMed PubMed Central

Murman, D.L. (2015). The impact of age on cognition. Semin. Hear. 36, 111–121. https://doi.org/10.1055/s-0035-1555115.Suche in Google Scholar PubMed PubMed Central

Murphy, C. (2019). Olfactory and other sensory impairments in Alzheimer disease. Nat. Rev. Neurol. 15, 11–24. https://doi.org/10.1038/s41582-018-0097-5.Suche in Google Scholar PubMed

Murphy, C., Jernigan, T.L., and Fennema-Notestine, C. (2003). Left hippocampal volume loss in Alzheimer’s disease is reflected in performance on odor identification: a structural MRI study. J. Int. Neuropsychol. Soc. 9, 459–471. https://doi.org/10.1017/S1355617703930116.Suche in Google Scholar PubMed

Nakamura, N.H., Fukunaga, M., and Oku, Y. (2018). Respiratory modulation of cognitive performance during the retrieval process. PLoS One 13, e0204021. https://doi.org/10.1371/journal.pone.0204021.Suche in Google Scholar PubMed PubMed Central

Neville, K.R., and Haberly, L.B. (2003). Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J. Neurophysiol. 90, 3921–3930. https://doi.org/10.1152/jn.00475.2003.Suche in Google Scholar PubMed

Padmanabhan, K., Osakada, F., Tarabrina, A., Kizer, E., Callaway, E.M., Gage, F.H., and Sejnowski, T.J. (2019). Centrifugal inputs to the main olfactory bulb revealed through whole brain circuit-mapping. Front. Neuroanat. 12, 115. https://doi.org/10.3389/fnana.2018.00115.Suche in Google Scholar PubMed PubMed Central

Persson, B.M., Ambrozova, V., Duncan, S., Wood, E.R., O’Connor, A.R., and Ainge, J.A. (2022). Lateral entorhinal cortex lesions impair odor-context associative memory in male rats. J. Neurosci. Res. 100, 1030–1046. https://doi.org/10.1002/jnr.25027.Suche in Google Scholar PubMed PubMed Central

Poo, C., Agarwal, G., Bonacchi, N., and Mainen, Z.F. (2022). Spatial maps in piriform cortex during olfactory navigation. Nature 601, 595–599. https://doi.org/10.1038/s41586-021-04242-3.Suche in Google Scholar PubMed

Rangel, L.M., Rueckemann, J.W., Riviere, P.D., Keefe, K.R., Porter, B.S., Heimbuch, I.S., Budlong, C.H., and Eichenbaum, H. (2016). Rhythmic coordination of hippocampal neurons during associative memory processing. Elife 5, e09849. https://doi.org/10.7554/eLife.09849.Suche in Google Scholar PubMed PubMed Central

Richter, M., Murtaza, N., Scharrenberg, R., White, S.H., Johanns, O., Walker, S., Yuen, R.K.C., Schwanke, B., Bedürftig, B., Henis, M., et al.. (2019). Altered TAOK2 activity causes autism-related neurodevelopmental and cognitive abnormalities through RhoA signaling. Mol. Psychiatr. 24, 1329–1350. https://doi.org/10.1038/s41380-018-0025-5.Suche in Google Scholar PubMed PubMed Central

Roesler, R., and McGaugh, J.L. (2022). The entorhinal cortex as a gateway for amygdala influences on memory consolidation. Neuroscience S0306-4522, 00037–9. https://doi.org/10.1016/j.neuroscience.2022.01.023.Suche in Google Scholar PubMed

Salimi, M., Tabasi, F., Abdolsamadi, M., Dehghan, S., Dehdar, K., Nazari, M., Javan, M., Mirnajafi-Zadeh, J., and Raoufy, M.R. (2022). Disrupted connectivity in the olfactory bulb-entorhinal cortex-dorsal hippocampus circuit is associated with recognition memory deficit in Alzheimer’s disease model. Sci. Rep. 12, 4394. https://doi.org/10.1038/s41598-022-08528-y.Suche in Google Scholar PubMed PubMed Central

Stranahan, A.M., and Mattson, M.P. (2010). Selective vulnerability of neurons in layer II of the entorhinal cortex during aging and Alzheimer’s disease. Neural Plast. 2010, 108190. https://doi.org/10.1155/2010/108190.Suche in Google Scholar PubMed PubMed Central

Symanski, C.A., Bladon, J.H., Kullberg, E.T., and Jadhav, S.P. (2021). Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making, BioRxiv 2020.06.08.140939. https://doi.org/10.1101/2020.06.08.140939.Suche in Google Scholar

Tort, A.B.L., Brankačk, J., and Draguhn, A. (2018). Respiration-entrained brain rhythms are global but often overlooked. Trends Neurosci. 41, 186–197. https://doi.org/10.1016/j.tins.2018.01.007.Suche in Google Scholar PubMed

Uchida, S., Shimada, C., Sakuma, N., Kagitani, F., Kan, A., and Awata, S. (2020). The relationship between olfaction and cognitive function in the elderly. J. Physiol. Sci. 70, 48. https://doi.org/10.1186/s12576-020-00777-8.Suche in Google Scholar PubMed

Uhlhaas, P.J., and Singer, W. (2006). Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155–168. https://doi.org/10.1016/j.neuron.2006.09.020.Suche in Google Scholar PubMed

Vandrey, B., Garden, D.L.F., Ambrozova, V., McClure, C., Nolan, M.F., and Ainge, J.A. (2020). Fan cells in layer 2 of the lateral entorhinal cortex are critical for episodic-like memory. Curr. Biol. 30, 169–175.e5 https://doi.org/10.1016/j.cub.2019.11.027.Suche in Google Scholar PubMed PubMed Central

Walz, A., Omura, M., and Mombaerts, P. (2006). Development and topography of the lateral olfactory tract in the mouse: imaging by genetically encoded and injected fluorescent markers. J. Neurobiol. 66, 835–846. https://doi.org/10.1002/neu.20266.Suche in Google Scholar PubMed

Wang, P.Y., Boboila, C., Chin, M., Higashi-Howard, A., Shamash, P., Wu, Z., Stein, N.P., Abbott, L.F., and Axel, R. (2020). Transient and persistent representations of odor value in prefrontal cortex. Neuron 108, 209–224.e6. https://doi.org/10.1016/j.neuron.2020.07.033.Suche in Google Scholar PubMed PubMed Central

Wilson, D.I.G., Watanabe, S., Milner, H., and Ainge, J.A. (2013). Lateral entorhinal cortex is necessary for associative but not nonassociative recognition memory. Hippocampus 23, 1280–1290. https://doi.org/10.1002/hipo.22165.Suche in Google Scholar PubMed PubMed Central

Witter, M.P., Doan, T.P., Jacobsen, B., Nilssen, E.S., and Ohara, S. (2017). Architecture of the entorhinal cortex A review of entorhinal anatomy in rodents with some comparative notes. Front. Syst. Neurosci. 11, 46. https://doi.org/10.3389/fnsys.2017.00046.Suche in Google Scholar PubMed PubMed Central

Xu, X., Song, L., Kringel, R., and Hanganu-Opatz, I.L. (2021). Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice. Nat. Commun. 12, 6810. https://doi.org/10.1038/s41467-021-27114-w.Suche in Google Scholar PubMed PubMed Central

Yahiaoui-Doktor, M., Luck, T., Riedel-Heller, S.G., Loeffler, M., Wirkner, K., and Engel, C. (2019). Olfactory function is associated with cognitive performance: results from the population-based LIFE-Adult-Study. Alzheimer’s Res. Ther. 11, 43. https://doi.org/10.1186/s13195-019-0494-z.Suche in Google Scholar PubMed PubMed Central

Yang, Q., Zhou, G., Noto, T., Templer, J.W., Schuele, S.U., Rosenow, J.M., Lane, G., and Zelano, C. (2022). Smell-induced gamma oscillations in human olfactory cortex are required for accurate perception of odor identity. PLoS Biol. 20, e3001509. https://doi.org/10.1371/journal.pbio.3001509.Suche in Google Scholar PubMed PubMed Central

Yu, Y., Burton, S.D., Tripathy, S.J., and Urban, N.N. (2015). Postnatal development attunes olfactory bulb mitral cells to high-frequency signaling. J. Neurophysiol. 114, 2830–2842. https://doi.org/10.1152/jn.00315.2015.Suche in Google Scholar PubMed PubMed Central

Zelano, C., Jiang, H., Zhou, G., Arora, N., Schuele, S., Rosenow, J., and Gottfried, J.A. (2016). Nasal respiration entrains human limbic oscillations and modulates cognitive function. J. Neurosci. 36, 12448–12467. https://doi.org/10.1523/JNEUROSCI.2586-16.2016.Suche in Google Scholar PubMed PubMed Central

Published Online: 2022-06-06
Published in Print: 2022-08-26

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