Успехи физиологических наук, 2023, T. 54, № 2, стр. 20-36
Роль гиппокампа в восприятии и запоминании запахов. Гипотетический нейронный механизм
И. Г. Силькис *
Институт высшей нервной деятельности и нейрофизиологии РАН
117485 Москва, Россия
* E-mail: isa-silkis@mail.ru
Поступила в редакцию 09.01.2023
После доработки 15.01.2023
Принята к публикации 25.01.2023
- EDN: PLMXCA
- DOI: 10.31857/S0301179823020078
Полные тексты статей выпуска доступны в ознакомительном режиме только авторизованным пользователям.
Аннотация
Предложен механизм взаимозависимого функционирования обонятельной и гиппокампальной нейронных сетей. В этом функционировании существенную роль играют длительные изменения эффективности связей между нейронами из этих сетей, а также из вентральной части базальных ганглиев, фронтальных областей коры, таламических ядер реуниенс и медиодорзального. Запахи участвуют в пространственном картировании и навигации, поскольку эти два вида информации обрабатываются одновременно и взаимозависимо. Предложенный механизм формирования отображений ассоциаций “запах–объект–место” в активности нейронов из разных полей гиппокампа может лежать в основе участия запахов в определении “полей места”. Поле СА2 гиппокампа вносит важный вклад в этот процесс, способствуя запоминанию и извлечению из памяти информации, связанной с запахами и с их расположением. Благодаря гиппокампальным проекциям в обонятельные структуры, в активности нейронов пириформной коры также формируются пространственные отображения окружающей среды. Согласно предлагаемому механизму, повреждения различных звеньев анализируемых цепей, как и ослабление нейрогенеза в зубчатой извилине и обонятельной луковице, должны ухудшать обоняние и память на запахи. Это следствие согласуется с обонятельным дефицитом при различных нейродегенеративных и вирусных заболеваниях, а также при старении.
Полные тексты статей выпуска доступны в ознакомительном режиме только авторизованным пользователям.
Список литературы
Силькис И.Г. Участие трисинаптического гиппокампального пути в формировании нейронных отображений ассоциаций “объект–место” (аналитический обзор) // Журн. высш. нерв. деят. 2009. Т. 59. № 6. С. 645.
Силькис И.Г. О роли базальных ганглиев в обработке сложных звуковых стимулов и слуховом внимании // Успехи физиол. наук. 2015. Т. 46. № 3. С. 76.
Силькис И.Г. Участие ядер гипоталамуса в формировании ассоциаций объект-место на нейронах поля СА2 гиппокампа (гипотетический механизм) // Журн. высш. нерв. деят. 2021. № 71. № 2. С. 147. https://doi.org/10.31857/S0044467721020106
Силькис И.Г. О сходстве механизмов обработки обонятельной, слуховой и зрительной информации в ЦНС (Гипотеза) // Нейрохимия. 2023. Т. 40. № 1. С. 1. https://doi.org/10.31857/S1027813323010193
Aikath D., Weible A.P., Rowland D.C., Kentros C.G. Role of self-generated odor cues in contextual representation // Hippocampus. 2014. V. 24. № 8. P. 1039. https://doi.org/10.1002/hipo.22289
Aimone J.B., Deng W., Gage F.H. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation // Neuron. 2011. V. 70. № 4. P. 589. https://doi.org/10.1016/j.neuron.2011.05.010
Alexander G.M., Farris S., Pirone J.R. et al. Social and novel contexts modify hippocampal CA2 representations of space // Nat. Commun. 2016. V. 7. P. 10300. https://doi.org/10.1038/ncomms10300
Aqrabawi A.J., Kim J.C. Olfactory memory representations are stored in the anterior olfactory nucleus // Nat. Commun. 2020. V. 11. № 1. P. 1246. https://doi.org/10.1038/s41467-020-15032-2
Aqrabawi A.J., Kim J.C. Hippocampal projections to the anterior olfactory nucleus differentially convey spatiotemporal information during episodic odour memory // Nat. Commun. 2018. V. 9. № 1. P. 2735. https://doi.org/10.1038/s41467-018-05131-6
Bannert M.M., Bartels A. Human V4 Activity Patterns Predict Behavioral Performance in Imagery of Object Color // J. Neurosci. 2018. V. 38. № 15. P. 3657. https://doi.org/10.1523/JNEUROSCI.2307-17.2018
Bayat A.H., Azimi H., Hassani Moghaddam M. et al. COVID-19 causes neuronal degeneration and reduces neurogenesis in human hippocampus // Apoptosis. 2022. V. 27. № 11-12. P. 852. https://doi.org/10.1007/s10495-022-01754-9
Benoy A., Dasgupta A., Sajikumar S. Hippocampal area CA2: an emerging modulatory gateway in the hippocampal circuit // Exp. Brain Res. 2018. V. 236. № 4. P. 919. https://doi.org/10.1007/s00221-018-5187-5
Bhasin G., Nair I.R. Dynamic Hippocampal CA2 Responses to Contextual Spatial Novelty // Front. Syst. Neurosci. 2022. V. 16. P. 923911. https://doi.org/10.3389/fnsys.2022.923911
Biella G., de Curtis M. Olfactory inputs activate the medial entorhinal cortex via the hippocampus // J. Neurophysiol. 2000. V. 83. № 4. P. 1924. https://doi.org/10.1152/jn.2000.83.4.1924
Bitter T., Siegert F., Gudziol H. et al. Gray matter alterations in parosmia // Neuroscience. 2011. V. 177. P. 177. https://doi.org/10.1016/j.neuroscience.2011.01.016
Bitzenhofer S.H., Westeinde E.A., Zhang H.B., Isaacson J.S. Rapid odor processing by layer 2 subcircuits in lateral entorhinal cortex // Elife. 2022. V. 11. e75065. https://doi.org/10.7554/eLife.75065
Boesveldt S., de Muinck Keizer R.J., Wolters E.Ch., Berendse H.W. Odor recognition memory is not independently impaired in Parkinson’s disease // J. Neural Transm. (Vienna). 2009. V. 116. № 5. P. 575. https://doi.org/10.1007/s00702-009-0208-y
Cassano T., Romano A., Macheda T. et al. Olfactory memory is impaired in a triple transgenic model of Alzheimer disease // Behav. Brain Res. 2011. V. 224. № 2. P. 408. https://doi.org/10.1016/j.bbr.2011.06.029
Cenquizca L.A., Swanson L.W. Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex // Brain Res. Rev. 2007. V. 56. № 1. P. 1. https://doi.org/10.1016/j.brainresrev.2007.05.002
Chaillan F.A., Roman F.S., Soumireu-Mourat B. Modulation of synaptic plasticity in the hippocampus and piriform cortex by physiologically meaningful olfactory cues in an olfactory association task // J. Physiol. Paris. 1996. V. 90. № 5–6. P. 343. https://doi.org/10.1016/s0928-4257(97)87916-8
Chapuis J., Cohen Y., He X. et al. Lateral entorhinal modulation of piriform cortical activity and fine odor discrimination // J. Neurosci. 2013. V. 33. № 33. P. 13449. https://doi.org/10.1523/JNEUROSCI.1387-13.2013
Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop // Neuron. 2010. V. 66. № 4. P. 560. https://doi.org/10.1016/j.neuron.2010.04.013
Dahmani L., Patel R.M., Yang Y. et al. An intrinsic association between olfactory identification and spatial memory in humans // Nat. Commun. 2018. V. 9. № 1. P. 4162. https://doi.org/10.1038/s41467-018-06569-4
Dasgupta A., Baby N., Krishna K. et al. Substance P induces plasticity and synaptic tagging/capture in rat hippocampal area CA2 // Proc. Natl. Acad. Sci. USA. 2017. V. 114. № 41. P. E8741. https://doi.org/10.1073/pnas.1711267114
Datiche F., Luppi P.H., Cattarelli M. Projection from nucleus reuniens thalami to piriform cortex: a tracing study in the rat // Brain Res. Bull. 1995. V. 38. № 1. P. 87. https://doi.org/10.1016/0361-9230(95)00075-p
De La Rosa-Prieto C., De Moya-Pinilla M., Saiz-Sanchez D. et al. Olfactory and cortical projections to bulbar and hippocampal adult-born neurons // Front. Neuroanat. 2015. V. 9. P. 4. https://doi.org/10.3389/fnana.2015.00004
Deshmukh S.S., Bhalla U.S. Representation of odor habituation and timing in the hippocampus // J. Neurosci. 2003. V. 23. № 5. P. 1903. https://doi.org/10.1523/JNEUROSCI.23-05-01903.2003
Eichenbaum H. Using olfaction to study memory // Ann. NY Acad. Sci. 1998. V. 855. P. 657. https://doi.org/10.1111/j.1749-6632.1998.tb10642.x
Eichenbaum H., Robitsek R.J. Olfactory memory: a bridge between humans and animals in models of cognitive aging // Ann. NY Acad. Sci. 2009. V. 1170. P. 658. https://doi.org/10.1111/j.1749-6632.2009.04012.x
Ferraris M., Cassel J.C., Pereira de Vasconcelos A., Stephan A., Quilichini P.P. The nucleus reuniens, a thalamic relay for cortico-hippocampal interaction in recent and remote memory consolidation // Neurosci. Biobehav. Rev. 2021. V. 125. P. 339. https://doi.org/10.1016/j.neubiorev.2021.02.025
Fischler-Ruiz W., Clark D.G., Joshi N.R. et al. Olfactory landmarks and path integration converge to form a cognitive spatial map // Neuron. 2021. V. 109. № 24. P. 4036. e5. https://doi.org/10.1016/j.neuron.2021.09.055
Galliot E., Comte A., Magnin E. et al. Effects of an ambient odor on brain activations during episodic retrieval of objects // Brain Imaging Behav. 2013. V. 7. № 2. P. 213. https://doi.org/10.1007/s11682-012-9218-8
Ge S., Yang C.H., Hsu K.S., Ming G.L., Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain // Neuron. 2007. V. 54. № 4. P. 559. https://doi.org/10.1016/j.neuron.2007.05.002
Gilbert P.E., Pirogovsky E., Ferdon S., Brushfield A.M., Murphy C. Differential effects of normal aging on memory for odor-place and object-place associations // Exp. Aging Res. 2008. V. 34. № 4. P. 437. https://doi.org/10.1080/03610730802271914
Gnatkovsky V., Uva L., de Curtis M. Topographic distribution of direct and hippocampus-mediated entorhinal cortex activity evoked by olfactory tract stimulation // Eur. J. Neurosci. 2004. V. 20. № 7. P. 1897. https://doi.org/10.1111/j.1460-9568.2004.03627.x
Goodrich-Hunsaker N.J., Gilbert P.E., Hopkins R.O. The role of the human hippocampus in odor-place associative memory // Chem. Senses. 2009. V. 34. № 6. P. 513. https://doi.org/10.1093/chemse/bjp026
Gottfried J.A., Smith A.P., Rugg M.D., Dolan R.J. Remembrance of odors past: human olfactory cortex in cross-modal recognition memory // Neuron. 2004. V. 42. № 4. P. 687. https://doi.org/10.1016/s0896-6273(04)00270-3
Gourévitch B., Kay L.M., Martin C. Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task // J. Neurophysiol. 2010. V. 103. № 5. P. 2633. https://doi.org/10.1152/jn.01075.2009
Grella S.L., Fortin A.H., McKissick O., Leblanc H., Ramirez S. Odor modulates the temporal dynamics of fear memory consolidation // Learn. Mem. 2020. V. 27. № 4. P. 150. https://doi.org/10.1101/lm.050690.119
Hanson E., Swanson J., Arenkiel B.R. Sensory experience shapes the integration of adult-born neurons into the olfactory bulb // J. Nat. Sci. 2017. V. 3. № 8. P. e422
Hitti F.L., Siegelbaum S.A. The hippocampal CA2 region is essential for social memory // Nature. 2014. V. 508. № 7494. P. 88. https://doi.org/10.1038/nature13028
Huang C.C., Rolls E.T., Hsu C.H., Feng J., Lin C.P. Extensive Cortical Connectivity of the Human Hippocampal Memory System: Beyond the “What” and “Where” Dual Stream Model // Cereb. Cortex. 2021. V. 31. № 10. P. 4652. https://doi.org/10.1093/cercor/bhab113
Insausti R., Marcos P., Arroyo-Jiménez M.M., Blaizot X., Martínez-Marcos A. Comparative aspects of the olfactory portion of the entorhinal cortex and its projection to the hippocampus in rodents, nonhuman primates, and the human brain // Brain Res. Bull. 2002. V. 57. № 3–4. P. 557. https://doi.org/10.1016/s0361-9230(01)00684-0
Jaako-Movits K., Zharkovsky A. Impaired fear memory and decreased hippocampal neurogenesis following olfactory bulbectomy in rats // Eur. J. Neurosci. 2005. V. 22. № 11. P. 2871. https://doi.org/10.1111/j.1460-9568.2005.04481.x
Jones-Gotman M., Zatorre R.J. Odor recognition memory in humans: role of right temporal and orbitofrontal regions // Brain Cogn. 1993. V. 22. № 2. P. 182. https://doi.org/10.1006/brcg.1993.1033
Jorge P.E., Phillips J.B., Gonçalves A., Marques P.A., Nĕmec P. Odours stimulate neuronal activity in the dorsolateral area of the hippocampal formation during path integration // Proc. Biol. Sci. 2014. V. 281. № 1783. P. 20140025. https://doi.org/10.1098/rspb.2014.0025
Kazarian A.L., Hekimian A.A., Harutiunian-Kozak B.A. et al. Responses of cat’s dorsal hippocampal neurones to moving visual stimuli // Acta. Neurobiol. Exp. (Wars). 1995. V. 55. № 2. P. 99
Kesner R.P., Hunsaker M.R., Ziegler W. The role of the dorsal and ventral hippocampus in olfactory working memory // Neurobiol. Learn. Mem. 2011. V. 96. № 2. P. 361. https://doi.org/10.1016/j.nlm.2011.06.011
Kim W.B., Cho J.H. Synaptic Targeting of Double-Projecting Ventral CA1 Hippocampal Neurons to the Medial Prefrontal Cortex and Basal Amygdala // J. Neurosci. 2017. V. 37. № 19. P. 4868. https://doi.org/10.1523/JNEUROSCI.3579-16.2017
Kjelvik G., Evensmoen H.R., Brezova V., Håberg A.K. The human brain representation of odor identification // J. Neurophysiol. 2012. V. 108. № 2. P. 645. https://doi.org/10.1152/jn.01036.2010
Knafo S., Ariav G., Barkai E., Libersat F. Olfactory learning-induced increase in spine density along the apical dendrites of CA1 hippocampal neurons // Hippocampus. 2004. V. 14. № 7. P. 819. https://doi.org/10.1002/hipo.10219
Künzle H. An extrahippocampal projection from the dentate gyrus to the olfactory tubercle // BMC Neurosci. 2005. V. 6. P. 38. https://doi.org/10.1186/1471-2202-6-38
Lavenex P., Amaral D.G. Hippocampal-neocortical interaction: a hierarchy of associativity // Hippocampus. 2000. V. 10. № 4. P.420. https://doi.org/10.1002/1098-1063(2000)10:4<420:: AID-HIPO8>3.0.CO;2-5
Lebedev M.A., Ossadtchi A. Commentary: Spatial Olfactory Learning Contributes to Place Field Formation in the Hippocampus // Front. Syst. Neurosci. 2018. V. 12. P. 8. https://doi.org/10.3389/fnsys.2018.00008
Lehr A.B., Kumar A., Tetzlaff C., Hafting T., Fyhn M., Stöber T.M. CA2 beyond social memory: Evidence for a fundamental role in hippocampal information processing // Neurosci. Biobehav. Rev. 2021. V. 126. P. 398. https://doi.org/10.1016/j.neubiorev.2021.03.020
Leitner F.C., Melzer S., Lütcke H. et al. Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex // Nat. Neurosci. 2016. V. 19. № 7. P. 935. https://doi.org/10.1038/nn.4303
Levinson M., Kolenda J.P., Alexandrou G.J. et al. Context-dependent odor learning requires the anterior olfactory nucleus // Behav. Neurosci. 2020. V. 134. № 4. P. 332. https://doi.org/10.1037/bne0000371
Levy D.A., Hopkins R.O., Squire L.R. Impaired odor recognition memory in patients with hippocampal lesions // Learn. Mem. 2004. V. 11. № 6. P. 794. https://doi.org/10.1101/lm.82504
Li Y., Xu J., Liu Y. et al. A distinct entorhinal cortex to hippocampal CA1 direct circuit for olfactory associative learning // Nat. Neurosci. 2017. V. 20. № 4. P. 559. https://doi.org/10.1038/nn.4517
Linley S.B., Gallo M.M., Vertes R.P. Lesions of the ventral midline thalamus produce deficits in reversal learning and attention on an odor texture set shifting task // Brain Res. 2016. V. 1649. Pt. A. P. 110. https://doi.org/10.1016/j.brainres.2016.08.022
Liu P., Bilkey D.K. Parallel involvement of perirhinal and lateral entorhinal cortex in the polysynaptic activation of hippocampus by olfactory inputs // Hippocampus. 1997. V. 7. № 3. P. 296. https://doi.org/10.1002/(SICI)1098-1063(1997)7:3<296:: AID-HIPO5>3.0.CO;2-J
Lunardi P., Mansk L.M.Z., Jaimes L.F., Pereira G.S. On the novel mechanisms for social memory and the emerging role of neurogenesis // Brain Res. Bull. 2021. V. 171. P. 56. https://doi.org/10.1016/j.brainresbull.2021.03.006
Ma D.K., Kim W.R., Ming G.L., Song H. Activity-dependent extrinsic regulation of adult olfactory bulb and hippocampal neurogenesis // Ann. NY Acad. Sci. 2009. V. 1170. P. 664. https://doi.org/10.1111/j.1749-6632.2009.04373.x
Ma Q., Rolls E.T., Huang C.C., Cheng W., Feng J. Extensive cortical functional connectivity of the human hippocampal memory system // Cortex. 2022. V. 147. P. 83. https://doi.org/10.1016/j.cortex.2021.11.014
MacDonald C.J., Carrow S., Place R., Eichenbaum H. Distinct hippocampal time cell sequences represent odor memories in immobilized rats // J. Neurosci. 2013. V. 33. P. 14607. https://doi.org/10.1523/JNEUROSCI.1537-13.2013
Mankin E.A., Diehl G.W., Sparks F.T., Leutgeb S., Leutgeb J.K. Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts // Neuron. 2015. V. 85. № 1. P. 190. https://doi.org/10.1016/j.neuron.2014.12.001
Masurkar A.V., Srinivas K.V., Brann D.H. et al. Medial and Lateral Entorhinal Cortex Differentially Excite Deep versus Superficial CA1 Pyramidal Neurons // Cell Rep. 2017. V. 18. № 1. P. 148. https://doi.org/10.1016/j.celrep.2016.12.012
Middleton S.J., McHugh T.J. CA2: A Highly Connected Intrahippocampal Relay // Annu. Rev. Neurosci. 2020. V. 43. P. 55. https://doi.org/10.1146/annurev-neuro-080719-100343
Mouly A.M., Di Scala G. Entorhinal cortex stimulation modulates amygdala and piriform cortex responses to olfactory bulb inputs in the rat // Neuroscience. 2006. V. 137. № 4. P. 1131. https://doi.org/10.1016/j.neuroscience.2005.10.024
Murray E.A., Wise S.P., Graham K.S. Representational specializations of the hippocampus in phylogenetic perspective // Neurosci. Lett. 2018. V. 680. P. 4. https://doi.org/10.1016/j.neulet.2017.04.065
Naber P.A., Lopes da Silva F.H., Witter M.P. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum // Hippocampus. 2001. V. 11. № 2. P. 99. https://doi.org/10.1002/hipo.1028
Nordin S., Murphy C. Odor memory in normal aging and Alzheimer’s disease // Ann. NY Acad. Sci. 1998. V. 855. P. 686. https://doi.org/10.1111/j.1749-6632.1998.tb10646.x
Otto T., Schottler F., Staubli U., Eichenbaum H., Lynch G. Hippocampus and olfactory discrimination learning: effects of entorhinal cortex lesions on olfactory learning and memory in a successive-cue, go-no-go task // Behav. Neurosci. 1991. V. 105. № 1. P. 111. https://doi.org/10.1037//0735-7044.105.1.111
Pang C.C., Kiecker C., O’Brien J.T., Noble W., Chang R.C. Ammon’s Horn 2 (CA2) of the Hippocampus: A Long-Known Region with a New Potential Role in Neurodegeneration // Neuroscientist. 2019. V. 25. № 2. P. 167. https://doi.org/10.1177/1073858418778747
Pereira-Caixeta A.R., Guarnieri L.O., Medeiros D.C. et al. Inhibiting constitutive neurogenesis compromises long-term social recognition memory // Neurobiol. Learn. Mem. 2018. V. 155. P. 92. https://doi.org/10.1016/j.nlm.2018.06.014
Persson B.M., Ambrozova V., Duncan S. et al. Lateral entorhinal cortex lesions impair odor-context associative memory in male rats // J. Neurosci. Res. 2022. V. 100. № 4. P. 1030. https://doi.org/10.1002/jnr.25027
Phillipson O.T., Griffiths A.C. The topographic order of inputs to nucleus accumbens in the rat // Neuroscience. 1985. V. 16. № 2. P. 275. https://doi.org/10.1016/0306-4522(85)90002-8
Poo C., Agarwal G., Bonacchi N., Mainen Z.F. Spatial maps in piriform cortex during olfactory navigation // Nature. 2022. V. 601. № 7894. P. 595. https://doi.org/10.1038/s41586-021-04242-3
Radhakrishnan R.K., Kandasamy M. SARS-CoV-2-Mediated Neuropathogenesis, Deterioration of Hippocampal Neurogenesis and Dementia // Am. J. Alzheimers Dis. Other Demen. 2022. V. 37. P. 15333175221078418. https://doi.org/10.1177/15333175221078418
Radvansky B.A., Oh J.Y., Climer J.R., Dombeck D.A. Behavior determines the hippocampal spatial mapping of a multisensory environment // Cell Rep. 2021. V. 36. № 5. P. 109444. https://doi.org/10.1016/j.celrep.2021.109444
Ramus S.J., Davis J.B., Donahue R.J., Discenza C.B., Waite A.A. Interactions between the orbitofrontal cortex and the hippocampal memory system during the storage of long-term memory // Ann. NY Acad. Sci. 2007. V. 1121. P. 216. https://doi.org/10.1196/annals.1401.038
Rethinavel H.S., Ravichandran S., Radhakrishnan R.K., Kandasamy M. COVID-19 and Parkinson’s disease: Defects in neurogenesis as the potential cause of olfactory system impairments and anosmia // J. Chem. Neuroanat. 2021. V. 115. P. 101965. https://doi.org/10.1016/j.jchemneu.2021.101965
Riceberg J.S., Srinivasan A., Guise K.G., Shapiro M.L. Hippocampal signals modify orbitofrontal representations to learn new paths // Curr. Biol. 2022. V. 32. № 15. P. 3407.e6. https://doi.org/10.1016/j.cub.2022.06.010
Robert V., Therreau L., Chevaleyre V. et al. Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1 // Elife. 2021. V. 10. P. e63352. https://doi.org/10.7554/eLife.63352
Robinson S., Granata L., Hienz R.D., Davis C.M. Temporary inactivation of the medial prefrontal cortex impairs the formation, but not the retrieval of social odor recognition memory in rats // Neurobiol. Learn. Mem. 2019. V. 161. P. 115. https://doi.org/10.1016/j.nlm.2019.04.003
Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory // J. Neurosci. 2002. V. 22. № 7. P. 2679. https://doi.org/10.1523/JNEUROSCI.22-07-02679.2002
Rolls E.T., Deco G., Huang C.C., Feng J. The effective connectivity of the human hippocampal memory system // Cereb. Cortex. 2022. V. 32. № 17. P. 3706. https://doi.org/10.1093/cercor/bhab442
Roman F.S., Truchet B., Chaillan F.A., Marchetti E., Soumireu-Mourat B. Olfactory associative discrimination: a model for studying modifications of synaptic efficacy in neuronal networks supporting long-term memory // Rev. Neurosci. 2004. V. 15. № 1. P. 1. https://doi.org/10.1515/revneuro.2004.15.1.1
Roullet P., Bourne R., Moricard Y., Stewart M.G., Sara S.J. Learning-induced plasticity of N-methyl-D-aspartate receptors is task and region specific // Neuroscience. 1999. V. 89. № 4. P. 1145. https://doi.org/10.1016/s0306-4522(98)00404-7
Russo M.J., Franks K.M., Oghaz R., Axel R., Siegelbaum S.A. Synaptic organization of anterior olfactory nucleus inputs to piriform cortex // J. Neurosci. 2020. V. 40. № 49. P. 9414. https://doi.org/10.1523/JNEUROSCI.0965-20.2020
Rusznák Z., Sengul G., Paxinos G., Kim W.S., Fu Y. Odor Enrichment Increases Hippocampal Neuron Numbers in Mouse // Exp. Neurobiol. 2018. V. 27. № 2. P. 94. https://doi.org/10.5607/en.2018.27.2.94
Sahay A., Wilson D.A., Hen R. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb // Neuron. 2011. V. 70. № 4. P. 582. https://doi.org/10.1016/j.neuron.2011.05.012
Saiz-Sanchez D., De La Rosa-Prieto C., Ubeda-Bañon I., Martinez-Marcos A. Interneurons and beta-amyloid in the olfactory bulb, anterior olfactory nucleus and olfactory tubercle in APPxPS1 transgenic mice model of Alzheimer’s disease // Anat. Rec (Hoboken). 2013. V. 296. № 9. P. 1413. https://doi.org/10.1002/ar.22750
Sakamoto M., Ieki N., Miyoshi G. et al. Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning // J. Neurosci. 2014. V. 34. № 17. P. 5788. https://doi.org/10.1523/JNEUROSCI.0674-14.2014
Schmidt-Hieber C., Jonas P., Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus // Nature. 2004. V. 429. № 6988. P. 184. https://doi.org/10.1038/nature02553
Schwerdtfeger W.K., Buhl E.H., Germroth P. Disynaptic olfactory input to the hippocampus mediated by stellate cells in the entorhinal cortex // J. Comp. Neurol. 1990. V. 292. № 2. P. 163. https://doi.org/10.1002/cne.902920202
Silkis I. A hypothetical role of cortico-basal ganglia-thalamocortical loops in visual processing // Biosystems. 2007. V. 89. № 1–3. P. 227. https://doi.org/10.1016/j.biosystems.2006.04.020
Soung A.L., Vanderheiden A., Nordvig A.S. et al. COVID-19 induces CNS cytokine expression and loss of hippocampal neurogenesis // Brain. 2022. V. 145. № 12. P. 4193. https://doi.org/10.1093/brain/awac270
Srinivas K.V., Buss E.W., Sun Q. et al. The Dendrites of CA2 and CA1 Pyramidal Neurons Differentially Regulate Information Flow in the Cortico-Hippocampal Circuit // J. Neurosci. 2017. V. 37. № 12. P. 3276. https://doi.org/10.1523/JNEUROSCI.2219-16.2017
Stevenson E.L., Caldwell H.K. Lesions to the CA2 region of the hippocampus impair social memory in mice // Eur. J. Neurosci. 2014. V. 40. № 9. P. 3294. https://doi.org/10.1111/ejn.12689
Strauch C., Hoang T.H., Angenstein F., Manahan-Vaughan D. Olfactory information storage engages subcortical and cortical brain regions that support valence determination // Cereb. Cortex. 2022. V. 32. № 4. P. 689. https://doi.org/10.1093/cercor/bhab226
Strauch C., Manahan-Vaughan D. In the piriform cortex, the primary impetus for information encoding through synaptic plasticity is provided by descending rather than ascending olfactory inputs // Cereb. Cortex. 2018. V. № 2. P. 764. https://doi.org/10.1093/cercor/bhx315
Syversen I.F., Witter M.P., Kobro-Flatmoen A. et al. Structural connectivity-based segmentation of the human entorhinal cortex // Neuroimage. 2021. V. 245. P. 18723. https://doi.org/10.1016/j.neuroimage.2021.118723
Taxidis J., Pnevmatikakis E.A., Dorian C.C. et al. Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences // Neuron. 2020. V. 108. № 5. P. 984.e9. https://doi.org/10.1016/j.neuron.2020.08.028
Tamamaki N., Nojyo Y. Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats // J. Comp. Neurol. 1995. V. 353. № 3. P. 379. https://doi.org/10.1002/cne.903530306
Traub R.D., Whittington M.A. Processing of cell assemblies in the lateral entorhinal cortex // Rev. Neurosci. 2022. V. 33. № 6. P. 829. https://doi.org/10.1515/revneuro-2022-0011
Truchet B., Chaillan F.A., Soumireu-Mourat B., Roman F.S. Early integrative processes physiologically observed in dentate gyrus during an olfactory associative training in rat // J. Integr. Neurosci. 2002. V. 1. № 1. P. 101. https://doi.org/10.1142/s0219635202000062
Truchet B., Chaillan F.A., Soumireu-Mourat B., Roman F.S. Learning and memory of cue-reward association meaning by modifications of synaptic efficacy in dentate gyrus and piriform cortex // Hippocampus. 2002. V. 12. № 5. P. 600. https://doi.org/10.1002/hipo.10097
Uva L., de Curtis M. Polysynaptic olfactory pathway to the ipsi- and contralateral entorhinal cortex mediated via the hippocampus // Neuroscience. 2005. V. 130. № 1. P. 249. https://doi.org/10.1016/j.neuroscience.2004.08.042
Vandenbroucke A.R.E., Fahrenfort J.J., Meuwese J.D.I., Scholte H.S., Lamme V.A.F. Prior Knowledge about Objects Determines Neural Color Representation in Human Visual Cortex // Cereb. Cortex. 2016. V. 26. № 4. P. 1401. https://doi.org/10.1093/cercor/bhu224
Vanderwolf C.H. The hippocampus as an olfacto-motor mechanism: were the classical anatomists right after all? // Behav. Brain Res. 2001. V. 127. № 1–2. P. 25. https://doi.org/10.1016/s0166-4328(01)00354-0
van Groen T., Wyss J.M. Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections // J. Comp. Neurol. 1990. V. 302. № 3. P. 515. https://doi.org/10.1002/cne.903020308
van Rijzingen I.M., Gispen W.H., Spruijt B.M. Olfactory bulbectomy temporarily impairs Morris maze performance: an ACTH (4–9) analog accellerates return of function // Physiol. Behav. 1995. V. 58. P. 147. https://doi.org/10.1016/0031-9384(95)00032-E
Weeden C.S., Hu N.J., Ho L.U., Kesner R.P. The role of the ventral dentate gyrus in olfactory pattern separation // Hippocampus. 2014. V. 24. № 5. P. 553. https://doi.org/10.1002/hipo.22248
Wilson R.S., Arnold S.E., Schneider J.A., Tang Y., Bennett D.A. The relationship between cerebral Alzheimer’s disease pathology and odour identification in old age // J. Neurol. Neurosurg. Psychiatry. 2007. V. 78. № 1. P. 30. https://doi.org/10.1136/jnnp.2006.099721
Wilson D.A., Stevenson R.J. The fundamental role of memory in olfactory perception // Trends Neurosci. 2003. V. 26. № 5. P. 243. https://doi.org/10.1016/S0166-2236(03)00076-6
Wilson D.I., Watanabe S., Milner H., Ainge J.A. Lateral entorhinal cortex is necessary for associative but not nonassociative recognition memory // Hippocampus. 2013. V. 23. № 12. P. 1280. https://doi.org/10.1002/hipo.22165
Woods N.I., Stefanini F., Apodaca-Montano D.L. et al. The Dentate Gyrus Classifies Cortical Representations of Learned Stimuli // Neuron. 2020. V. 107. № 1. P. 173.e6. https://doi.org/10.1016/j.neuron.2020.04.002
Xu W., Lopez-Guzman M., Schoen C. et al. Spared piriform cortical single-unit odor processing and odor discrimination in the Tg2576 mouse model of Alzheimer’s disease // PLoS One. 2014. V. 9. № 9. P. e106431. https://doi.org/10.1371/journal.pone.0106431
Xu W., Wilson D.A. Odor-evoked activity in the mouse lateral entorhinal cortex // Neuroscience. 2012. V. 223. P. 12. https://doi.org/10.1016/j.neuroscience.2012.07.067
Yamamoto T. Involvement of the olfactory system in learning and memory: a close correlation between the olfactory deficit and the course of Alzheimer’s disease? // Yakubutsu Seishin Kodo. 1991. V. 11. № 4. P. 223
Yoder W.M., Gaynor L.S., Burke S.N. et al. Interaction between age and perceptual similarity in olfactory discrimination learning in F344 rats: relationships with spatial learning // Neurobiol. Aging. 2017. V. 53. P. 122. https://doi.org/10.1016/j.neurobiolaging.2017.01.023
Zhang S., Manahan-Vaughan D. Spatial olfactory learning contributes to place field formation in the hippocampus // Cereb. Cortex. 2015. V. 25. № 2. P. 423. https://doi.org/10.1093/cercor/bht239
Zheng J.Q. Cortical projections from the reuniens nucleus of the thalamus in the rat // Kaibogaku Zasshi. 1994. V. 69. № 3. P. 261
Zhou G., Olofsson J.K., Koubeissi M.Z. et al. Human hippocampal connectivity is stronger in olfaction than other sensory systems // Prog. Neurobiol. 2021. V. 201. P. 102027. https://doi.org/10.1016/j.pneurobio.2021.102027
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