П’ять відкриттів Володимира Беца. Частина перша. Бец і острови енторінальної кори

  • Володимир Медведєв Кафедра нейрохірургії НМУ імені О.О. Богомольця, Київ, Україна https://orcid.org/0000-0001-7236-3191
  • Віктор Черкасов Кафедра описової та клінічної анатомії НМУ імені О.О. Богомольця, Київ, Україна https://orcid.org/0000-0001-9920-9047
  • Вікторія Васлович Відділ нейропатоморфології, Державна Установа «Інститут нейрохірургії ім. акад. А.П. Ромоданова НАМН України», Київ, Україна https://orcid.org/0000-0002-7503-4745
  • Віталій Цимбалюк Кафедра нейрохірургії НМУ імені О.О. Богомольця, Київ, Україна https://orcid.org/0000-0003-3608-9679
Ключові слова: історія медицини, нейронауки, енторінальна кора, клітини решітки, епізодична пам’ять, сприйняття часу, хвороба Альцгеймера

Анотація

у серії публікацій, котру відкриває ця стаття, ми розглядаємо п’ять фундаментальних нейроморфологічних спостережень нашого співвітчизника, класика світової нейронауки Володимра Беца. Для чотирьох із них ми вперше демонструємо статус відкриттів, для іншого одного — гігантських пірамідних нейронів рухової кори — попри повсюдне і давнє його визнання, розкриваємо обмеженість сучасних знань і уявлень. Два із згаданих спостережень — гігантські веретеноподібні нейрони поясної й острівцевої кори і острови енторінальної кори — наданий час відомі лише вузькому колу фахівців; на решту два, острови Калеха і ознаки колонкової організації кори — ми звертаємо увагу вперше. У цій, початковій частині циклу, розкриваючи сучасні уявлення про будову і функції енторінальної кори, ми демонструємо вагу першоспостереження Бецом непересічних нейронних кластерів, відомих зараз як енторінальні острови, доводимо факт визнання його історичного пріоритету у описанні цих дивовижних структур мозку.

Посилання

Abraham, W. C., Jones, O. D., & Glanzman, D. L. (2019). Is plasticity of synapses the mechanism of long-term memory storage?. NPJ science of learning, 4, 9. https://doi.org/10.1038/s41539-019-0048-y

Agmon, H., & Burak, Y. (2020). A theory of joint attractor dynamics in the hippocampus and the entorhinal cortex accounts for artificial remapping and grid cell field-to-field variability. eLife, 9, e56894. https://doi.org/10.7554/eLife.56894

Altschul, R. (1933) Die Glomeruli der Area praesubicularis. Zeitschrift für die gesamte Neurologie und Psychiatrie, 148(1), 50–54. https://doi.org/10.1007/BF02865159

Amani, M., Lauterborn, J. C., Le, A. A., Cox, B. M., Wang, W., Quintanilla, J. et al. (2021). Rapid Aging in the Perforant Path Projections to the Rodent Dentate Gyrus. The Journal of neuroscience : the official journal of the Society for Neuroscience, 41(10), 2301–2312. https://doi.org/10.1523/JNEUROSCI.2376-20.2021

Amaral, D. G., Insausti, R., & Cowan, W. M. (1987). The entorhinal cortex of the monkey: I. Cytoarchitectonic organization. The Journal of comparative neurology, 264(3), 326–355. https://doi.org/10.1002/cne.902640305

Angelaki, D. E., & Laurens, J. (2020). The head direction cell network: attractor dynamics, integration within the navigation system, and three-dimensional properties. Current opinion in neurobiology, 60, 136–144. https://doi.org/10.1016/j.conb.2019.12.002

Azevedo, E. P., Pomeranz, L., Cheng, J., Schneeberger, M., Vaughan, R., Stern, S. A., Tan, B., Doerig, K., Greengard, P., & Friedman, J. M. (2019). A Role of Drd2 Hippocampal Neurons in Context-Dependent Food Intake. Neuron, 102(4), 873–886.e5. https://doi.org/10.1016/j.neuron.2019.03.011

Bareš, M., Apps, R., Avanzino, L., Breska, A., D'Angelo, E., Filip, P., Gerwig, M., Ivry, R. B., Lawrenson, C. L., Louis, E. D., Lusk, N. A., Manto, M., Meck, W. H., Mitoma, H., & Petter, E. A. (2019). Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications. Cerebellum (London, England), 18(2), 266–286. https://doi.org/10.1007/s12311-018-0979-5

Beall, M. J., & Lewis, D. A. (1992). Heterogeneity of layer II neurons in human entorhinal cortex. The Journal of comparative neurology, 321(2), 241–266. https://doi.org/10.1002/cne.903210206

Bellmund, J. L., Deuker, L., & Doeller, C. F. (2019). Mapping sequence structure in the human lateral entorhinal cortex. eLife, 8, e45333. https://doi.org/10.7554/eLife.45333

Bellmund, J. L., Deuker, L., Navarro Schröder, T., & Doeller, C. F. (2016). Grid-cell representations in mental simulation. eLife, 5, e17089. https://doi.org/10.7554/eLife.17089

Bellmund, J., de Cothi, W., Ruiter, T. A., Nau, M., Barry, C., & Doeller, C. F. (2020). Deforming the metric of cognitive maps distorts memory. Nature human behaviour, 4(2), 177–188. https://doi.org/10.1038/s41562-019-0767-3

Bellmund, J., Deuker, L., Montijn, N. D., & Doeller, C. F. (2022). Mnemonic construction and representation of temporal structure in the hippocampal formation. Nature communications, 13(1), 3395. https://doi.org/10.1038/s41467-022-30984-3

Bellmund, J., Polti, I., & Doeller, C. F. (2020). Sequence Memory in the Hippocampal-Entorhinal Region. Journal of cognitive neuroscience, 32(11), 2056–2070. https://doi.org/10.1162/jocn_a_01592

Betz, V. A. (1882). O podrobnostyakh stroyeniya mozgovoy korki cheloveka: predvaritel'noye soobshcheniye (posvyashchayetsya pamyati professora parizhskogo meditsinskogo fakul'teta Polya Broka). [On the details of the human cerebral cortex structure: a preliminary report (dedicated to the memory of Paul Broca, professor at the Parisian Faculty of Medicine)]. In Zapiski Kíevskоgo Obshchestva Yestestvoispytateley [Notes of the Kiev Society of Naturalists] (Vol. 6, issue 2, p. 165–176). Kyiv: Printing House Ern. Perlis. http://ukr.catalogue.nlu.org.ua/?page=2&arg2=записки киевского

Betz, W. (1881). Ueber die feinere Struktur der Gehirnrinde des Menschen. Centralblatt Fuer Die Medizinischen Wissenschaften, 19(11), 193–195; 19(12), 209–213; 19(13), 231–233. https://archive.org/details/bub_gb_acADAAAAYAAJ/page/192/mode/2up

Bitzenhofer, S. H., Westeinde, E. A., Zhang, H. B., & 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

Bliss, T. V., & Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. The Journal of physiology, 232(2), 331–356. https://doi.org/10.1113/jphysiol.1973.sp010273

Bliss, T., & Collingridge, G. L. (2019). Persistent memories of long-term potentiation and the N-methyl-d-aspartate receptor. Brain and neuroscience advances, 3, 2398212819848213. https://doi.org/10.1177/2398212819848213

Boccara, C. N., Nardin, M., Stella, F., O'Neill, J., & Csicsvari, J. (2019). The entorhinal cognitive map is attracted to goals. Science (New York, N.Y.), 363(6434), 1443–1447. https://doi.org/10.1126/science.aav4837.

Braak H. (1972). Zur Pigmentarchitektonik der Grosshirnrinde des Menschen. I. Regio entorhinalis [Pigmentarchitecture of the human cortex cerebri. I. Regio entorhinalis]. Zeitschrift fur Zellforschung und mikroskopische Anatomie (Vienna, Austria : 1948), 127(3), 407–438. https://doi.org/10.1007/BF00306883

Braden, B. B., & Riecken, C. (2019). Thinning Faster? Age-Related Cortical Thickness Differences in Adults with Autism Spectrum Disorder. Research in autism spectrum disorders, 64, 31–38. https://doi.org/10.1016/j.rasd.2019.03.005

Bright, I. M., Meister, M., Cruzado, N. A., Tiganj, Z., Buffalo, E. A., & Howard, M. W. (2020). A temporal record of the past with a spectrum of time constants in the monkey entorhinal cortex. Proceedings of the National Academy of Sciences of the United States of America, 117(33), 20274–20283. https://doi.org/10.1073/pnas.1917197117

Butti, C., & Hof, P. R. (2010). The insular cortex: a comparative perspective. Brain structure & function, 214(5-6), 477–493. https://doi.org/10.1007/s00429-010-0264-y

Butti, C., Ewan Fordyce, R., Ann Raghanti, M., Gu, X., Bonar, C. J., Wicinski, B. A., Wong, E. W., Roman, J., Brake, A., Eaves, E., Spocter, M. A., Tang, C. Y., Jacobs, B., Sherwood, C. C., & Hof, P. R. (2014). The cerebral cortex of the pygmy hippopotamus, Hexaprotodon liberiensis (Cetartiodactyla, Hippopotamidae): MRI, cytoarchitecture, and neuronal morphology. Anatomical record (Hoboken, N.J. : 2007), 297(4), 670–700. https://doi.org/10.1002/ar.22875

Campbell, M. G., & Giocomo, L. M. (2018). Self-motion processing in visual and entorhinal cortices: inputs, integration, and implications for position coding. Journal of neurophysiology, 120(4), 2091–2106. https://doi.org/10.1152/jn.00686.2017

Chen, D., Kunz, L., Wang, W., Zhang, H., Wang, W. X., Schulze-Bonhage, A. et al. (2018). Hexadirectional Modulation of Theta Power in Human Entorhinal Cortex during Spatial Navigation. Current biology : CB, 28(20), 3310–3315.e4. https://doi.org/10.1016/j.cub.2018.08.029

Chen, L. L., Lin, L. H., Green, E. J., Barnes, C. A., & McNaughton, B. L. (1994). Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Experimental brain research, 101(1), 8–23. https://doi.org/10.1007/BF00243212

Chen, X., Vieweg, P., & Wolbers, T. (2019). Computing distance information from landmarks and self-motion cues - Differential contributions of anterior-lateral vs. posterior-medial entorhinal cortex in humans. NeuroImage, 202, 116074. https://doi.org/10.1016/j.neuroimage.2019.116074

Cona, G., & Scarpazza, C. (2019). Where is the "where" in the brain? A meta-analysis of neuroimaging studies on spatial cognition. Human brain mapping, 40(6), 1867–1886. https://doi.org/10.1002/hbm.24496

Connor, C. E., & Knierim, J. J. (2017). Integration of objects and space in perception and memory. Nature neuroscience, 20(11), 1493–1503. https://doi.org/10.1038/nn.4657

Constantinescu, A. O., O'Reilly, J. X., & Behrens, T. (2016). Organizing conceptual knowledge in humans with a gridlike code. Science (New York, N.Y.), 352(6292), 1464–1468. https://doi.org/10.1126/science.aaf0941

D'Albis, T., & Kempter, R. (2020). Recurrent amplification of grid-cell activity. Hippocampus, 30(12), 1268–1297. https://doi.org/10.1002/hipo.23254

Dandolo, L. C., & Schwabe, L. (2018). Time-dependent memory transformation along the hippocampal anterior-posterior axis. Nature communications, 9(1), 1205. https://doi.org/10.1038/s41467-018-03661-7

Dang, R., Zhou, Y., Zhang, Y., Liu, D., Wu, M., Liu, A., Jia, Z., & Xie, W. (2022). Regulation of Social Memory by Lateral Entorhinal Cortical Projection to Dorsal Hippocampal CA2. Neuroscience bulletin, 38(3), 318–322. https://doi.org/10.1007/s12264-021-00813-6

Danjo, T., Toyoizumi, T., & Fujisawa, S. (2018). Spatial representations of self and other in the hippocampus. Science (New York, N.Y.), 359(6372), 213–218. https://doi.org/10.1126/science.aao3898

Deshmukh, S. S., & Knierim, J. J. (2011). Representation of non-spatial and spatial information in the lateral entorhinal cortex. Frontiers in behavioral neuroscience, 5, 69. https://doi.org/10.3389/fnbeh.2011.00069

Deuker, L., Bellmund, J. L., Navarro Schröder, T., & Doeller, C. F. (2016). An event map of memory space in the hippocampus. eLife, 5, e16534. https://doi.org/10.7554/eLife.16534

Dias, M., Ferreira, R., & Remondes, M. (2021). Medial Entorhinal Cortex Excitatory Neurons Are Necessary for Accurate Timing. The Journal of neuroscience : the official journal of the Society for Neuroscience, 41(48), 9932–9943. https://doi.org/10.1523/JNEUROSCI.0750-21.2021

Diehl, G. W., Hon, O. J., Leutgeb, S., & Leutgeb, J. K. (2017). Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes. Neuron, 94(1), 83–92.e6. https://doi.org/10.1016/j.neuron.2017.03.004

Ding S. L. (2013). Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. The Journal of comparative neurology, 521(18), 4145–4162. https://doi.org/10.1002/cne.23416

Doan, T. P., Lagartos-Donate, M. J., Nilssen, E. S., Ohara, S., & Witter, M. P. (2019). Convergent Projections from Perirhinal and Postrhinal Cortices Suggest a Multisensory Nature of Lateral, but Not Medial, Entorhinal Cortex. Cell reports, 29(3), 617–627.e7. https://doi.org/10.1016/j.celrep.2019.09.005

Doeller, C. F., Barry, C., & Burgess, N. (2010). Evidence for grid cells in a human memory network. Nature, 463(7281), 657–661. https://doi.org/10.1038/nature08704

Dringenberg H. C. (2020). The history of long-term potentiation as a memory mechanism: Controversies, confirmation, and some lessons to remember. Hippocampus, 30(9), 987–1012. https://doi.org/10.1002/hipo.23213

East, B. S., Jr, Brady, L. R., & Quinn, J. J. (2021). Differential Effects of Lateral and Medial Entorhinal Cortex Lesions on Trace, Delay and Contextual Fear Memories. Brain sciences, 12(1), 34. https://doi.org/10.3390/brainsci12010034

Eichenbaum H. (2017). On the Integration of Space, Time, and Memory. Neuron, 95(5), 1007–1018. https://doi.org/10.1016/j.neuron.2017.06.036

Ekstrom, A. D., Harootonian, S. K., & Huffman, D. J. (2020). Grid coding, spatial representation, and navigation: Should we assume an isomorphism?. Hippocampus, 30(4), 422–432. https://doi.org/10.1002/hipo.23175

Fernández-Ruiz, A., Oliva, A., Soula, M., Rocha-Almeida, F., Nagy, G. A., Martin-Vazquez, G., & Buzsáki, G. (2021). Gamma rhythm communication between entorhinal cortex and dentate gyrus neuronal assemblies. Science (New York, N.Y.), 372(6537), eabf3119. https://doi.org/10.1126/science.abf3119

Finkelstein, A., Derdikman, D., Rubin, A., Foerster, J. N., Las, L., & Ulanovsky, N. (2015). Three-dimensional head-direction coding in the bat brain. Nature, 517(7533), 159–164. https://doi.org/10.1038/nature14031

Fyhn, M., Hafting, T., Treves, A., Moser, M. B., & Moser, E. I. (2007). Hippocampal remapping and grid realignment in entorhinal cortex. Nature, 446(7132), 190–194. https://doi.org/10.1038/nature05601

Gardner, R. J., Hermansen, E., Pachitariu, M., Burak, Y., Baas, N. A., Dunn, B. A., Moser, M. B., & Moser, E. I. (2022). Toroidal topology of population activity in grid cells. Nature, 602(7895), 123–128. https://doi.org/10.1038/s41586-021-04268-7

Ginosar, G., Aljadeff, J., Burak, Y., Sompolinsky, H., Las, L., & Ulanovsky, N. (2021). Locally ordered representation of 3D space in the entorhinal cortex. Nature, 596(7872), 404–409. https://doi.org/10.1038/s41586-021-03783-x

Giocomo, L. M., Stensola, T., Bonnevie, T., Van Cauter, T., Moser, M. B., & Moser, E. I. (2014). Topography of head direction cells in medial entorhinal cortex. Current biology : CB, 24(3), 252–262. https://doi.org/10.1016/j.cub.2013.12.002

Gómez-Isla, T., Price, J. L., McKeel, D. W., Jr, Morris, J. C., Growdon, J. H., & Hyman, B. T. (1996). Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. The Journal of neuroscience : the official journal of the Society for Neuroscience, 16(14), 4491–4500. https://doi.org/10.1523/JNEUROSCI.16-14-04491.1996

Gryglewski, G., Murgaš, M., Klöbl, M., Reed, M. B., Unterholzner, J., Michenthaler, P., & Lanzenberger, R. (2022). Enrichment of Disease-Associated Genes in Cortical Areas Defined by Transcriptome-Based Parcellation. Biological psychiatry. Cognitive neuroscience and neuroimaging, 7(1), 10–23. https://doi.org/10.1016/j.bpsc.2021.02.012

Gu, Y., Lewallen, S., Kinkhabwala, A. A., Domnisoru, C., Yoon, K., Gauthier, J. L., Fiete, I. R., & Tank, D. W. (2018). A Map-like Micro-Organization of Grid Cells in the Medial Entorhinal Cortex. Cell, 175(3), 736–750.e30. https://doi.org/10.1016/j.cell.2018.08.066

Guida, F., Iannotta, M., Misso, G., Ricciardi, F., Boccella, S., Tirino, V., Falco, M., Desiderio, V., Infantino, R., Pieretti, G., de Novellis, V., Papaccio, G., Luongo, L., Caraglia, M., & Maione, S. (2022). Long-term neuropathic pain behaviors correlate with synaptic plasticity and limbic circuit alteration: a comparative observational study in mice. Pain, 163(8), 1590–1602. https://doi.org/10.1097/j.pain.0000000000002549

Guthman, E. M., Garcia, J. D., Ma, M., Chu, P., Baca, S. M., Smith, K. R., Restrepo, D., & Huntsman, M. M. (2020). Cell-type-specific control of basolateral amygdala neuronal circuits via entorhinal cortex-driven feedforward inhibition. eLife, 9, e50601. https://doi.org/10.7554/eLife.50601

Hafting, T., Fyhn, M., Molden, S., Moser, M. B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801–806. https://doi.org/10.1038/nature03721

Hardcastle, K., Ganguli, S., & Giocomo, L. M. (2017). Cell types for our sense of location: where we are and where we are going. Nature neuroscience, 20(11), 1474–1482. https://doi.org/10.1038/nn.4654

Haug F. M. (1976). Sulphide silver pattern and cytoarchitectonics of parahippocampal areas in the rat. Special reference to the subdivision of area entorhinalis (area 28) and its demarcation from the pyriform cortex. Advances in anatomy, embryology, and cell biology, 52(4), 3–73.

He, Q., & Brown, T. I. (2019). Environmental Barriers Disrupt Grid-like Representations in Humans during Navigation. Current biology : CB, 29(16), 2718–2722.e3. https://doi.org/10.1016/j.cub.2019.06.072.

Heinsen, H., Henn, R., Eisenmenger, W., Götz, M., Bohl, J., Bethke, B. et al. (1994). Quantitative investigations on the human entorhinal area: left-right asymmetry and age-related changes. Anatomy and embryology, 190(2), 181–194. https://doi.org/10.1007/BF00193414

Hevner, R. F., & Wong-Riley, M. T. (1992). Entorhinal cortex of the human, monkey, and rat: metabolic map as revealed by cytochrome oxidase. The Journal of comparative neurology, 326(3), 451–469. https://doi.org/10.1002/cne.903260310

Hinman, J. R., Brandon, M. P., Climer, J. R., Chapman, G. W., & Hasselmo, M. E. (2016). Multiple Running Speed Signals in Medial Entorhinal Cortex. Neuron, 91(3), 666–679. https://doi.org/10.1016/j.neuron.2016.06.027

Hof, P. R., & Van der Gucht, E. (2007). Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anatomical record (Hoboken, N.J. : 2007), 290(1), 1–31. https://doi.org/10.1002/ar.20407

Horner, A. J., Bisby, J. A., Zotow, E., Bush, D., & Burgess, N. (2016). Grid-like Processing of Imagined Navigation. Current biology : CB, 26(6), 842–847. https://doi.org/10.1016/j.cub.2016.01.042

Horton, J. C., & Adams, D. L. (2005). The cortical column: a structure without a function. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 360(1456), 837–862. https://doi.org/10.1098/rstb.2005.1623

Høydal, Ø. A., Skytøen, E. R., Andersson, S. O., Moser, M. B., & Moser, E. I. (2019). Object-vector coding in the medial entorhinal cortex. Nature, 568(7752), 400–404. https://doi.org/10.1038/s41586-019-1077-7

Hu, J. M., Chen, C. H., Chen, S. Q., & Ding, S. L. (2020). Afferent Projections to Area Prostriata of the Mouse. Frontiers in neuroanatomy, 14, 605021. https://doi.org/10.3389/fnana.2020.605021

Huang, C. C., Rolls, E. T., Hsu, C. H., Feng, J., & Lin, C. P. (2021). Extensive Cortical Connectivity of the Human Hippocampal Memory System: Beyond the "What" and "Where" Dual Stream Model. Cerebral cortex (New York, N.Y. : 1991), 31(10), 4652–4669. https://doi.org/10.1093/cercor/bhab113

Igarashi K. M. (2015). Plasticity in oscillatory coupling between hippocampus and cortex. Current opinion in neurobiology, 35, 163–168. https://doi.org/10.1016/j.conb.2015.09.005

Igarashi K. M. (2016). The entorhinal map of space. Brain research, 1637, 177–187. https://doi.org/10.1016/j.brainres.2015.10.041

Igarashi, K. M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W. R., & Mori, K. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience, 32(23), 7970–7985. https://doi.org/10.1523/JNEUROSCI.0154-12.2012

Igarashi, K. M., Lu, L., Colgin, L. L., Moser, M. B., & Moser, E. I. (2014). Coordination of entorhinal-hippocampal ensemble activity during associative learning. Nature, 510(7503), 143–147. https://doi.org/10.1038/nature13162

Insausti, R., & Amaral, D. G. (2008). Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents. The Journal of comparative neurology, 509(6), 608–641. https://doi.org/10.1002/cne.21753

Insausti, R., & Amaral, D. G. (2012). Hippocampal formation. In J. Mai, & G. Paxinos (Eds.), The human nervous system (3rd ed.). (pp. 896–942). San Diego: Academic Press. https://doi.org/10.1016/B978-0-12-374236-0.10024-0

Insausti, R., Amaral, D. G., & Cowan, W. M. (1987). The entorhinal cortex of the monkey: II. Cortical afferents. The Journal of comparative neurology, 264(3), 356–395. https://doi.org/10.1002/cne.902640306

Insausti, R., Insausti, A. M., Sobreviela, M. T., Salinas, A., & Martínez-Peñuela, J. M. (1998). Human medial temporal lobe in aging: anatomical basis of memory preservation. Microscopy research and technique, 43(1), 8–15. https://doi.org/10.1002/(SICI)1097-0029(19981001)43:1<8::AID-JEMT2>3.0.CO;2-4

Insausti, R., Muñoz-López, M., Insausti, A. M., & Artacho-Pérula, E. (2017). The Human Periallocortex: Layer Pattern in Presubiculum, Parasubiculum and Entorhinal Cortex. A Review. Frontiers in neuroanatomy, 11, 84. https://doi.org/10.3389/fnana.2017.00084

Insausti, R., Tuñón, T., Sobreviela, T., Insausti, A. M., & Gonzalo, L. M. (1995). The human entorhinal cortex: a cytoarchitectonic analysis. The Journal of comparative neurology, 355(2), 171–198. https://doi.org/10.1002/cne.903550203

Ionov, I. D., Pushinskaya, I. I., Gorev, N. P., & Frenkel, D. D. (2020). Cyclosomatostatin-induced catalepsy in aged rats: Specific change of brain c-Fos protein expression in the lateral entorhinal cortex. Brain research bulletin, 159, 79–86. https://doi.org/10.1016/j.brainresbull.2020.03.013

Ionov, I. D., Pushinskaya, I. I., Gorev, N. P., Frenkel, D. D., & Severtsev, N. N. (2021). Anticataleptic activity of nicotine in rats: involvement of the lateral entorhinal cortex. Psychopharmacology, 238(9), 2471–2483. https://doi.org/10.1007/s00213-021-05870-3

Ionov, I. D., Pushinskaya, I. I., Gorev, N. P., Shpilevaya, L. A., Frenkel, D. D., & Severtsev, N. N. (2021). Histamine H1 receptors regulate anhedonic-like behavior in rats: Involvement of the anterior cingulate and lateral entorhinal cortices. Behavioural brain research, 412, 113445. https://doi.org/10.1016/j.bbr.2021.113445

Ismakov, R., Barak, O., Jeffery, K., & Derdikman, D. (2017). Grid Cells Encode Local Positional Information. Current biology : CB, 27(15), 2337–2343.e3. https://doi.org/10.1016/j.cub.2017.06.034

Jacob, P. Y., Capitano, F., Poucet, B., Save, E., & Sargolini, F. (2019). Path integration maintains spatial periodicity of grid cell firing in a 1D circular track. Nature communications, 10(1), 840. https://doi.org/10.1038/s41467-019-08795-w

Jacob, P. Y., Poucet, B., Liberge, M., Save, E., & Sargolini, F. (2014). Vestibular control of entorhinal cortex activity in spatial navigation. Frontiers in integrative neuroscience, 8, 38. https://doi.org/10.3389/fnint.2014.00038

Jacobs, J., Kahana, M. J., Ekstrom, A. D., Mollison, M. V., & Fried, I. (2010). A sense of direction in human entorhinal cortex. Proceedings of the National Academy of Sciences of the United States of America, 107(14), 6487–6492. https://doi.org/10.1073/pnas.0911213107

Jayakumar, R. P., Madhav, M. S., Savelli, F., Blair, H. T., Cowan, N. J., & Knierim, J. J. (2019). Recalibration of path integration in hippocampal place cells. Nature, 566(7745), 533–537. https://doi.org/10.1038/s41586-019-0939-3

Joshi, V. V., Patel, N. D., Rehan, M. A., & Kuppa, A. (2019). Mysterious Mechanisms of Memory Formation: Are the Answers Hidden in Synapses?. Cureus, 11(9), e5795. https://doi.org/10.7759/cureus.5795

Julian, J. B., Keinath, A. T., Frazzetta, G., & Epstein, R. A. (2018). Human entorhinal cortex represents visual space using a boundary-anchored grid. Nature neuroscience, 21(2), 191–194. https://doi.org/10.1038/s41593-017-0049-1

Kang, L., & Balasubramanian, V. (2019). A geometric attractor mechanism for self-organization of entorhinal grid modules. eLife, 8, e46687. https://doi.org/10.7554/eLife.46687

Kaplan, R., & Friston, K. J. (2019). Entorhinal transformations in abstract frames of reference. PLoS biology, 17(5), e3000230. https://doi.org/10.1371/journal.pbio.3000230

Kelley, P., Evans, M., & Kelley, J. (2018). Making Memories: Why Time Matters. Frontiers in human neuroscience, 12, 400. https://doi.org/10.3389/fnhum.2018.00400

Khan, I. S., D'Agostino, E. N., Calnan, D. R., Lee, J. E., & Aronson, J. P. (2019). Deep Brain Stimulation for Memory Modulation: A New Frontier. World neurosurgery, 126, 638–646. https://doi.org/10.1016/j.wneu.2018.12.184

Killian, N. J., Jutras, M. J., & Buffalo, E. A. (2012). A map of visual space in the primate entorhinal cortex. Nature, 491(7426), 761–764. https://doi.org/10.1038/nature11587

Kim, M., & Maguire, E. A. (2019). Can we study 3D grid codes non-invasively in the human brain? Methodological considerations and fMRI findings. NeuroImage, 186, 667–678. https://doi.org/10.1016/j.neuroimage.2018.11.041

Kinkhabwala, A. A., Gu, Y., Aronov, D., & Tank, D. W. (2020). Visual cue-related activity of cells in the medial entorhinal cortex during navigation in virtual reality. eLife, 9, e43140. https://doi.org/10.7554/eLife.43140

Kitamura T. (2017). Driving and regulating temporal association learning coordinated by entorhinal-hippocampal network. Neuroscience research, 121, 1–6. https://doi.org/10.1016/j.neures.2017.04.005

Kobro-Flatmoen, A., & Witter, M. P. (2019). Neuronal chemo-architecture of the entorhinal cortex: A comparative review. The European journal of neuroscience, 50(10), 3627–3662. https://doi.org/10.1111/ejn.14511

Kobro-Flatmoen, A., Lagartos-Donate, M. J., Aman, Y., Edison, P., Witter, M. P., & Fang, E. F. (2021). Re-emphasizing early Alzheimer's disease pathology starting in select entorhinal neurons, with a special focus on mitophagy. Ageing research reviews, 67, 101307. https://doi.org/10.1016/j.arr.2021.101307

Kordower, J. H., Chu, Y., Stebbins, G. T., DeKosky, S. T., Cochran, E. J., Bennett, D. et al. (2001). Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Annals of neurology, 49(2), 202–213.

Krishna, A., Mittal, D., Virupaksha, S. G., Nair, A. R., Narayanan, R., & Thakur, C. S. (2021). Biomimetic FPGA-based spatial navigation model with grid cells and place cells. Neural networks : the official journal of the International Neural Network Society, 139, 45–63. https://doi.org/10.1016/j.neunet.2021.01.028

Kropff, E., Carmichael, J. E., Moser, M. B., & Moser, E. I. (2015). Speed cells in the medial entorhinal cortex. Nature, 523(7561), 419–424. https://doi.org/10.1038/nature14622

Krupic, J., Bauza, M., Burton, S., & O'Keefe, J. (2018). Local transformations of the hippocampal cognitive map. Science (New York, N.Y.), 359(6380), 1143–1146. https://doi.org/10.1126/science.aao4960

Krupic, J., Bauza, M., Burton, S., Barry, C., & O'Keefe, J. (2015). Grid cell symmetry is shaped by environmental geometry. Nature, 518(7538), 232–235. https://doi.org/10.1038/nature14153

Kunz, L., Brandt, A., Reinacher, P. C., Staresina, B. P., Reifenstein, E. T., Weidemann, C. T., Herweg, N. A., Patel, A., Tsitsiklis, M., Kempter, R., Kahana, M. J., Schulze-Bonhage, A., & Jacobs, J. (2021). A neural code for egocentric spatial maps in the human medial temporal lobe. Neuron, 109(17), 2781–2796.e10. https://doi.org/10.1016/j.neuron.2021.06.019

Kuruvilla, M. V., Wilson, D., & Ainge, J. A. (2020). Lateral entorhinal cortex lesions impair both egocentric and allocentric object-place associations. Brain and neuroscience advances, 4, 2398212820939463. https://doi.org/10.1177/2398212820939463

Lin, C., Oh, M. M., & Disterhoft, J. F. (2022). Aging-Related Alterations to Persistent Firing in the Lateral Entorhinal Cortex Contribute to Deficits in Temporal Associative Memory. Frontiers in aging neuroscience, 14, 838513. https://doi.org/10.3389/fnagi.2022.838513

Lin, C., Sherathiya, V. N., Oh, M. M., & Disterhoft, J. F. (2020). Persistent firing in LEC III neurons is differentially modulated by learning and aging. eLife, 9, e56816. https://doi.org/10.7554/eLife.56816

Liu S. (2020). Dopamine Suppresses Synaptic Responses of Fan Cells in the Lateral Entorhinal Cortex to Olfactory Bulb Input in Mice. Frontiers in cellular neuroscience, 14, 181. https://doi.org/10.3389/fncel.2020.00181

Llamas-Rodríguez, J., Oltmer, J., Greve, D. N., Williams, E., Slepneva, N., Wang, R., Champion, S., Lang-Orsini, M., Fischl, B., Frosch, M. P., van der Kouwe, A., & Augustinack, J. C. (2022). Entorhinal Subfield Vulnerability to Neurofibrillary Tangles in Aging and the Preclinical Stage of Alzheimer's Disease. Journal of Alzheimer's disease : JAD, 87(3), 1379–1399. https://doi.org/10.3233/JAD-215567

Lømo, T. (1966). Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiologica Scandinavica, 68 (Suppl. 277), 128. The source is cited according to: https://en.wikipedia.org/wiki/Long-term_potentiation.

Lopez-Rojas, J., de Solis, C. A., Leroy, F., Kandel, E. R., & Siegelbaum, S. A. (2022). A direct lateral entorhinal cortex to hippocampal CA2 circuit conveys social information required for social memory. Neuron, 110(9), 1559–1572.e4. https://doi.org/10.1016/j.neuron.2022.01.028

Luo, W., Yun, D., Hu, Y., Tian, M., Yang, J., Xu, Y., Tang, Y., Zhan, Y., Xie, H., & Guan, J. S. (2022). Acquiring new memories in neocortex of hippocampal-lesioned mice. Nature communications, 13(1), 1601. https://doi.org/10.1038/s41467-022-29208-5

Mahnke, L., Atucha, E., Pina-Fernàndez, E., Kitsukawa, T., & Sauvage, M. M. (2021). Lesion of the hippocampus selectively enhances LEC's activity during recognition memory based on familiarity. Scientific reports, 11(1), 19085. https://doi.org/10.1038/s41598-021-98509-4

Maidenbaum, S., Miller, J., Stein, J. M., & Jacobs, J. (2018). Grid-like hexadirectional modulation of human entorhinal theta oscillations. Proceedings of the National Academy of Sciences of the United States of America, 115(42), 10798–10803. https://doi.org/10.1073/pnas.1805007115

Matsumoto, N., Kitanishi, T., & Mizuseki, K. (2019). The subiculum: Unique hippocampal hub and more. Neuroscience research, 143, 1–12. https://doi.org/10.1016/j.neures.2018.08.002

Mau, W., Sullivan, D. W., Kinsky, N. R., Hasselmo, M. E., Howard, M. W., & Eichenbaum, H. (2018). The Same Hippocampal CA1 Population Simultaneously Codes Temporal Information over Multiple Timescales. Current biology : CB, 28(10), 1499–1508.e4. https://doi.org/10.1016/j.cub.2018.03.051

Meier, A. M., Wang, Q., Ji, W., Ganachaud, J., & Burkhalter, A. (2021). Modular Network between Postrhinal Visual Cortex, Amygdala, and Entorhinal Cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience, 41(22), 4809–4825. https://doi.org/10.1523/JNEUROSCI.2185-20.2021

Miao, C., Cao, Q., Moser, M. B., & Moser, E. I. (2017). Parvalbumin and Somatostatin Interneurons Control Different Space-Coding Networks in the Medial Entorhinal Cortex. Cell, 171(3), 507–521.e17. https://doi.org/10.1016/j.cell.2017.08.050

Mikkonen, M., Soininen, H., & Pitkänen, A. (1997). Distribution of parvalbumin-, calretinin-, and calbindin-D28k-immunoreactive neurons and fibers in the human entorhinal cortex. The Journal of comparative neurology, 388(1), 64–88. https://doi.org/10.5115/acb.2017.50.3.230

Mizumori, S. J., & Williams, J. D. (1993). Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. The Journal of neuroscience : the official journal of the Society for Neuroscience, 13(9), 4015–4028. https://doi.org/10.1523/JNEUROSCI.13-09-04015.1993

Montchal, M. E., Reagh, Z. M., & Yassa, M. A. (2019). Precise temporal memories are supported by the lateral entorhinal cortex in humans. Nature neuroscience, 22(2), 284–288. https://doi.org/10.1038/s41593-018-0303-1

Moon, H. J., Gauthier, B., Park, H. D., Faivre, N., & Blanke, O. (2022). Sense of self impacts spatial navigation and hexadirectional coding in human entorhinal cortex. Communications biology, 5(1), 406. https://doi.org/10.1038/s42003-022-03361-5

Moser, E. I., Moser, M. B., & McNaughton, B. L. (2017). Spatial representation in the hippocampal formation: a history. Nature neuroscience, 20(11), 1448–1464. https://doi.org/10.1038/nn.4653

Mosheiff, N., & Burak, Y. (2019). Velocity coupling of grid cell modules enables stable embedding of a low dimensional variable in a high dimensional neural attractor. eLife, 8, e48494. https://doi.org/10.7554/eLife.48494

Nau, M., Navarro Schröder, T., Bellmund, J., & Doeller, C. F. (2018). Hexadirectional coding of visual space in human entorhinal cortex. Nature neuroscience, 21(2), 188–190. https://doi.org/10.1038/s41593-017-0050-8

Naumann, R. K., Preston-Ferrer, P., Brecht, M., & Burgalossi, A. (2018). Structural modularity and grid activity in the medial entorhinal cortex. Journal of neurophysiology, 119(6), 2129–2144. https://doi.org/10.1152/jn.00574.2017

Naumann, R. K., Ray, S., Prokop, S., Las, L., Heppner, F. L., & Brecht, M. (2016). Conserved size and periodicity of pyramidal patches in layer 2 of medial/caudal entorhinal cortex. The Journal of comparative neurology, 524(4), 783–806. https://doi.org/10.1002/cne.23865

Navarro Schröder, T., Haak, K. V., Zaragoza Jimenez, N. I., Beckmann, C. F., & Doeller, C. F. (2015). Functional topography of the human entorhinal cortex. eLife, 4, e06738. https://doi.org/10.7554/eLife.06738

Nilssen, E. S., Doan, T. P., Nigro, M. J., Ohara, S., & Witter, M. P. (2019). Neurons and networks in the entorhinal cortex: A reappraisal of the lateral and medial entorhinal subdivisions mediating parallel cortical pathways. Hippocampus, 29(12), 1238–1254. https://doi.org/10.1002/hipo.23145

Nilssen, E. S., Jacobsen, B., Fjeld, G., Nair, R. R., Blankvoort, S., Kentros, C., & Witter, M. P. (2018). Inhibitory Connectivity Dominates the Fan Cell Network in Layer II of Lateral Entorhinal Cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience, 38(45), 9712–9727. https://doi.org/10.1523/JNEUROSCI.1290-18.2018

Nosheny, R. L., Insel, P. S., Mattsson, N., Tosun, D., Buckley, S., Truran, D. et al. (2019). Associations among amyloid status, age, and longitudinal regional brain atrophy in cognitively unimpaired older adults. Neurobiology of aging, 82, 110–119. https://doi.org/10.1016/j.neurobiolaging.2019.07.005

Obenhaus, H. A., Zong, W., Jacobsen, R. I., Rose, T., Donato, F., Chen, L., Cheng, H., Bonhoeffer, T., Moser, M. B., & Moser, E. I. (2022). Functional network topography of the medial entorhinal cortex. Proceedings of the National Academy of Sciences of the United States of America, 119(7), e2121655119. https://doi.org/10.1073/pnas.2121655119

Ohara, S., Gianatti, M., Itou, K., Berndtsson, C. H., Doan, T. P., Kitanishi, T., Mizuseki, K., Iijima, T., Tsutsui, K. I., & Witter, M. P. (2019). Entorhinal Layer II Calbindin-Expressing Neurons Originate Widespread Telencephalic and Intrinsic Projections. Frontiers in systems neuroscience, 13, 54. https://doi.org/10.3389/fnsys.2019.00054

Ohara, S., Onodera, M., Simonsen, Ø. W., Yoshino, R., Hioki, H., Iijima, T., Tsutsui, K. I., & Witter, M. P. (2018). Intrinsic Projections of Layer Vb Neurons to Layers Va, III, and II in the Lateral and Medial Entorhinal Cortex of the Rat. Cell reports, 24(1), 107–116. https://doi.org/10.1016/j.celrep.2018.06.014

Ohara, S., Yoshino, R., Kimura, K., Kawamura, T., Tanabe, S., Zheng, A., Nakamura, S., Inoue, K. I., Takada, M., Tsutsui, K. I., & Witter, M. P. (2021). Laminar Organization of the Entorhinal Cortex in Macaque Monkeys Based on Cell-Type-Specific Markers and Connectivity. Frontiers in neural circuits, 15, 790116. https://doi.org/10.3389/fncir.2021.790116

O'Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain research, 34(1), 171–175. https://doi.org/10.1016/0006-8993(71)90358-1

Olajide, O. J., Suvanto, M. E., & Chapman, C. A. (2021). Molecular mechanisms of neurodegeneration in the entorhinal cortex that underlie its selective vulnerability during the pathogenesis of Alzheimer's disease. Biology open, 10(1), bio056796. https://doi.org/10.1242/bio.056796

O'Mara, S. M., & Aggleton, J. P. (2019). Space and Memory (Far) Beyond the Hippocampus: Many Subcortical Structures Also Support Cognitive Mapping and Mnemonic Processing. Frontiers in neural circuits, 13, 52. https://doi.org/10.3389/fncir.2019.00052

Omer, D. B., Maimon, S. R., Las, L., & Ulanovsky, N. (2018). Social place-cells in the bat hippocampus. Science (New York, N.Y.), 359(6372), 218–224. https://doi.org/10.1126/science.aao3474

Park, S. W., Jang, H. J., Kim, M., & Kwag, J. (2019). Spatiotemporally random and diverse grid cell spike patterns contribute to the transformation of grid cell to place cell in a neural network model. PloS one, 14(11), e0225100. https://doi.org/10.1371/journal.pone.0225100

Peng, L., Zeng, L. L., Liu, Q., Wang, L., Qin, J., Xu et al. (2018). Functional connectivity changes in the entorhinal cortex of taxi drivers. Brain and behavior, 8(9), e01022. https://doi.org/10.1002/brb3.1022

Persson, B. M., Ambrozova, V., Duncan, S., Wood, E. R., O'Connor, A. R., & Ainge, J. A. (2022). Lateral entorhinal cortex lesions impair odor-context associative memory in male rats. Journal of neuroscience research, 100(4), 1030–1046. https://doi.org/10.1002/jnr.25027

Pilkiw, M., Jarovi, J., & Takehara-Nishiuchi, K. (2022). Lateral Entorhinal Cortex Suppresses Drift in Cortical Memory Representations. The Journal of neuroscience : the official journal of the Society for Neuroscience, 42(6), 1104–1118. https://doi.org/10.1523/JNEUROSCI.1439-21.2021

Poitreau, J., Buttet, M., Manrique, C., Poucet, B., Sargolini, F., & Save, E. (2021). Navigation using global or local reference frames in rats with medial and lateral entorhinal cortex lesions. Behavioural brain research, 413, 113448. https://doi.org/10.1016/j.bbr.2021.113448

Price, J. L., Ko, A. I., Wade, M. J., Tsou, S. K., McKeel, D. W., & Morris, J. C. (2001). Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Archives of neurology, 58(9), 1395–1402. https://doi.org/10.1001/archneur.58.9.1395

Raghanti, M. A., Spurlock, L. B., Treichler, F. R., Weigel, S. E., Stimmelmayr, R., Butti, C., Thewissen, J. G., & Hof, P. R. (2015). An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls. Brain structure & function, 220(4), 2303–2314. https://doi.org/10.1007/s00429-014-0792-y

Raghanti, M. A., Wicinski, B., Meierovich, R., Warda, T., Dickstein, D. L., Reidenberg, J. S., Tang, C. Y., George, J. C., Hans Thewissen, J., Butti, C., & Hof, P. R. (2019). A Comparison of the Cortical Structure of the Bowhead Whale (Balaena mysticetus), a Basal Mysticete, with Other Cetaceans. Anatomical record (Hoboken, N.J. : 2007), 302(5), 745–760. https://doi.org/10.1002/ar.23991

Raithel, C. U., & Gottfried, J. A. (2021). What are grid-like responses doing in the orbitofrontal cortex?. Behavioral neuroscience, 135(2), 218–225. https://doi.org/10.1037/bne0000453

Ramon y Cajal, S. (1988). Studies on the human cerebral cortex IV: structure of the olfactory cerebral cortex of man and mammals. In J. DeFelipe & E. G. Jones (Eds.), Cajal on the cerebral cortex: An annotated translation of the complete writings (pр. 289–362). New York: Oxford University Press.

Ray, S., Naumann, R., Burgalossi, A., Tang, Q., Schmidt, H., & Brecht, M. (2014). Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science (New York, N.Y.), 343(6173), 891–896. https://doi.org/10.1126/science.1243028

Robertson, R. G., Rolls, E. T., & Georges-François, P. (1998). Spatial view cells in the primate hippocampus: effects of removal of view details. Journal of neurophysiology, 79(3), 1145–1156. https://doi.org/10.1152/jn.1998.79.3.1145

Rochefort, C., Lefort, J. M., & Rondi-Reig, L. (2013). The cerebellum: a new key structure in the navigation system. Frontiers in neural circuits, 7, 35. https://doi.org/10.3389/fncir.2013.00035

Rockland K. S. (2021). Cytochrome oxidase "blobs": a call for more anatomy. Brain structure & function, 226(9), 2793–2806. https://doi.org/10.1007/s00429-021-02360-2

Rodríguez-Domínguez, U., & Caplan, J. B. (2019). A hexagonal Fourier model of grid cells. Hippocampus, 29(1), 37–45. https://doi.org/10.1002/hipo.23028

Rolls E. T. (2018). The storage and recall of memories in the hippocampo-cortical system. Cell and tissue research, 373(3), 577–604. https://doi.org/10.1007/s00441-017-2744-3

Rolls E. T. (2021). Neurons including hippocampal spatial view cells, and navigation in primates including humans. Hippocampus, 31(6), 593–611. https://doi.org/10.1002/hipo.23324

Rolls, E. T., & Mills, P. (2019). The Generation of Time in the Hippocampal Memory System. Cell reports, 28(7), 1649–1658.e6. https://doi.org/10.1016/j.celrep.2019.07.042

Rowland, D. C., Obenhaus, H. A., Skytøen, E. R., Zhang, Q., Kentros, C. G., Moser, E. I. et al. (2018). Functional properties of stellate cells in medial entorhinal cortex layer II. eLife, 7, e36664. https://doi.org/10.7554/eLife.36664

Rueckemann, J. W., Sosa, M., Giocomo, L. M., & Buffalo, E. A. (2021). The grid code for ordered experience. Nature reviews. Neuroscience, 22(10), 637–649. https://doi.org/10.1038/s41583-021-00499-9

Salz, D. M., Tiganj, Z., Khasnabish, S., Kohley, A., Sheehan, D., Howard, M. W., & Eichenbaum, H. (2016). Time Cells in Hippocampal Area CA3. The Journal of neuroscience : the official journal of the Society for Neuroscience, 36(28), 7476–7484. https://doi.org/10.1523/JNEUROSCI.0087-16.2016

Sarel, A., Finkelstein, A., Las, L., & Ulanovsky, N. (2017). Vectorial representation of spatial goals in the hippocampus of bats. Science (New York, N.Y.), 355(6321), 176–180. https://doi.org/10.1126/science.aak9589

Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B. L., Witter, M. P., Moser, M. B., & Moser, E. I. (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science (New York, N.Y.), 312(5774), 758–762. https://doi.org/10.1126/science.1125572

Save, E., & Sargolini, F. (2017). Disentangling the Role of the MEC and LEC in the Processing of Spatial and Non-Spatial Information: Contribution of Lesion Studies. Frontiers in systems neuroscience, 11, 81. https://doi.org/10.3389/fnsys.2017.00081

Savelli, F., Yoganarasimha, D., & Knierim, J. J. (2008). Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus, 18(12), 1270–1282. https://doi.org/10.1002/hipo.20511

Schafer, M., & Schiller, D. (2018). Navigating Social Space. Neuron, 100(2), 476–489. https://doi.org/10.1016/j.neuron.2018.10.006

Sekeres, M. J., Winocur, G., & Moscovitch, M. (2018). The hippocampus and related neocortical structures in memory transformation. Neuroscience letters, 680, 39–53. https://doi.org/10.1016/j.neulet.2018.05.006

Shinder, M. E., & Taube, J. S. (2019). Three-dimensional tuning of head direction cells in rats. Journal of neurophysiology, 121(1), 4–37. https://doi.org/10.1152/jn.00880.2017

Shine, J. P., Valdés-Herrera, J. P., Tempelmann, C., & Wolbers, T. (2019). Evidence for allocentric boundary and goal direction information in the human entorhinal cortex and subiculum. Nature communications, 10(1), 4004. https://doi.org/10.1038/s41467-019-11802-9

Simic, G., Bexheti, S., Kelovic, Z., Kos, M., Grbic, K., Hof, P. R., & Kostovic, I. (2005). Hemispheric asymmetry, modular variability and age-related changes in the human entorhinal cortex. Neuroscience, 130(4), 911–925. https://doi.org/10.1016/j.neuroscience.2004.09.040

Singleton, E., Hansson, O., Pijnenburg, Y., La Joie, R., Mantyh, W. G., Tideman, P. et al. (2021). Heterogeneous distribution of tau pathology in the behavioural variant of Alzheimer's disease. Journal of neurology, neurosurgery, and psychiatry, 92(8), 872–880. Advance online publication. https://doi.org/10.1136/jnnp-2020-325497

Solodkin, A., & Van Hoesen, G. W. (1996). Entorhinal cortex modules of the human brain. The Journal of comparative neurology, 365(4), 610–617. https://doi.org/10.1002/(SICI)1096-9861(19960219)365:4<610::AID-CNE8>3.0.CO;2-7

Solstad, T., Boccara, C. N., Kropff, E., Moser, M. B., & Moser, E. I. (2008). Representation of geometric borders in the entorhinal cortex. Science (New York, N.Y.), 322(5909), 1865–1868. https://doi.org/10.1126/science.1166466

Spalla, D., Dubreuil, A., Rosay, S., Monasson, R., & Treves, A. (2019). Can Grid Cell Ensembles Represent Multiple Spaces?. Neural computation, 31(12), 2324–2347. https://doi.org/10.1162/neco_a_01237

Spalla, D., Treves, A., & Boccara, C. N. (2022). Angular and linear speed cells in the parahippocampal circuits. Nature communications, 13(1), 1907. https://doi.org/10.1038/s41467-022-29583-z

Stackman, R. W., & Taube, J. S. (1998). Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. The Journal of neuroscience : the official journal of the Society for Neuroscience, 18(21), 9020–9037. https://doi.org/10.1523/JNEUROSCI.18-21-09020.1998

Staudigl, T., Leszczynski, M., Jacobs, J., Sheth, S. A., Schroeder, C. E., Jensen, O., & Doeller, C. F. (2018). Hexadirectional Modulation of High-Frequency Electrophysiological Activity in the Human Anterior Medial Temporal Lobe Maps Visual Space. Current biology : CB, 28(20), 3325–3329.e4. https://doi.org/10.1016/j.cub.2018.09.035

Stephan, H. (1975). Allocortex. Berlin: Springer-Verlag.

Sugar, J., & Moser, M. B. (2019). Episodic memory: Neuronal codes for what, where, and when. Hippocampus, 29(12), 1190–1205. https://doi.org/10.1002/hipo.23132

Sun, C., Kitamura, T., Yamamoto, J., Martin, J., Pignatelli, M., Kitch, L. J., Schnitzer, M. J., & Tonegawa, S. (2015). Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. Proceedings of the National Academy of Sciences of the United States of America, 112(30), 9466–9471. https://doi.org/10.1073/pnas.1511668112

Suthana, N., Haneef, Z., Stern, J., Mukamel, R., Behnke, E., Knowlton, B., & Fried, I. (2012). Memory enhancement and deep-brain stimulation of the entorhinal area. The New England journal of medicine, 366(6), 502–510. https://doi.org/10.1056/NEJMoa1107212

Suzuki, W. A., & Porteros, A. (2002). Distribution of calbindin D-28k in the entorhinal, perirhinal, and parahippocampal cortices of the macaque monkey. The Journal of comparative neurology, 451(4), 392–412. https://doi.org/10.1002/cne.10370

Syversen, I. F., Witter, M. P., Kobro-Flatmoen, A., Goa, P. E., Navarro Schröder, T., & Doeller, C. F. (2021). Structural connectivity-based segmentation of the human entorhinal cortex. NeuroImage, 245, 118723. https://doi.org/10.1016/j.neuroimage.2021.118723

Takehara-Nishiuchi K. (2022). Neuronal Code for Episodic Time in the Lateral Entorhinal Cortex. Frontiers in integrative neuroscience, 16, 899412. https://doi.org/10.3389/fnint.2022.899412

Tang, Q., Burgalossi, A., Ebbesen, C. L., Ray, S., Naumann, R., Schmidt, H., Spicher, D., & Brecht, M. (2014). Pyramidal and stellate cell specificity of grid and border representations in layer 2 of medial entorhinal cortex. Neuron, 84(6), 1191–1197. https://doi.org/10.1016/j.neuron.2014.11.009

Tang, Q., Burgalossi, A., Ebbesen, C. L., Ray, S., Naumann, R., Schmidt, H. et al. (2014). Pyramidal and stellate cell specificity of grid and border representations in layer 2 of medial entorhinal cortex. Neuron, 84(6), 1191–1197. https://doi.org/10.1016/j.neuron.2014.11.009

Tang, Q., Ebbesen, C. L., Sanguinetti-Scheck, J. I., Preston-Ferrer, P., Gundlfinger, A., Winterer, J., Beed, P., Ray, S., Naumann, R., Schmitz, D., Brecht, M., & Burgalossi, A. (2015). Anatomical Organization and Spatiotemporal Firing Patterns of Layer 3 Neurons in the Rat Medial Entorhinal Cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience, 35(36), 12346–12354. https://doi.org/10.1523/JNEUROSCI.0696-15.2015

Taube J. S. (1995). Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. The Journal of neuroscience : the official journal of the Society for Neuroscience, 15(1 Pt 1), 70–86. https://doi.org/10.1523/JNEUROSCI.15-01-00070.1995

Taube, J. (2009). Head direction cells. Scholarpedia, 4(12), 1787, doi:10.4249/scholarpedia.1787, http://www.scholarpedia.org/article/Head_direction_cells

Taube, J. S., Muller, R. U., & Ranck, J. B., Jr (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. The Journal of neuroscience : the official journal of the Society for Neuroscience, 10(2), 420–435. https://doi.org/10.1523/JNEUROSCI.10-02-00420.1990

Taube, J. S., Muller, R. U., & Ranck, J. B., Jr (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. The Journal of neuroscience : the official journal of the Society for Neuroscience, 10(2), 436–447. https://doi.org/10.1523/JNEUROSCI.10-02-00436.1990

Tran, T. T., Speck, C. L., Gallagher, M., & Bakker, A. (2022). Lateral entorhinal cortex dysfunction in amnestic mild cognitive impairment. Neurobiology of aging, 112, 151–160. https://doi.org/10.1016/j.neurobiolaging.2021.12.008

Tsao, A., Moser, M. B., & Moser, E. I. (2013). Traces of experience in the lateral entorhinal cortex. Current biology : CB, 23(5), 399–405. https://doi.org/10.1016/j.cub.2013.01.036

Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J. J., Moser, M. B., & Moser, E. I. (2018). Integrating time from experience in the lateral entorhinal cortex. Nature, 561(7721), 57–62. https://doi.org/10.1038/s41586-018-0459-6

Tukker, J. J., Beed, P., Brecht, M., Kempter, R., Moser, E. I., & Schmitz, D. (2022). Microcircuits for spatial coding in the medial entorhinal cortex. Physiological reviews, 102(2), 653–688. https://doi.org/10.1152/physrev.00042.2020

Van Hoesen, G. W., Augustinack, J. C., Dierking, J., Redman, S. J., & Thangavel, R. (2000). The parahippocampal gyrus in Alzheimer's disease. Clinical and preclinical neuroanatomical correlates. Annals of the New York Academy of Sciences, 911, 254–274. https://doi.org/10.1111/j.1749-6632.2000.tb06731.x

Van Hoesen, G. W., Pandya, D. N., & Butters, N. (1972). Cortical afferents to the entorhinal cortex of the Rhesus monkey. Science (New York, N.Y.), 175(4029), 1471–1473. https://doi.org/10.1126/science.175.4029.1471

Vandrey, B., Duncan, S., & Ainge, J. A. (2021). Object and object-memory representations across the proximodistal axis of CA1. Hippocampus, 31(8), 881–896. https://doi.org/10.1002/hipo.23331

Vandrey, B., Garden, D., Ambrozova, V., McClure, C., Nolan, M. F., & Ainge, J. A. (2020). Fan Cells in Layer 2 of the Lateral Entorhinal Cortex Are Critical for Episodic-like Memory. Current biology : CB, 30(1), 169–175.e5. https://doi.org/10.1016/j.cub.2019.11.027

Vinepinsky, E., Perchik, S., & Segev, R. (2020). A Generalized Linear Model of a Navigation Network. Frontiers in neural circuits, 14, 56. https://doi.org/10.3389/fncir.2020.00056

Vo, A., Tabrizi, N. S., Hunt, T., Cayanan, K., Chitale, S., Anderson, L. G., Tenney, S., White, A. O., Sabariego, M., & Hales, J. B. (2021). Medial entorhinal cortex lesions produce delay-dependent disruptions in memory for elapsed time. Neurobiology of learning and memory, 185, 107507. https://doi.org/10.1016/j.nlm.2021.107507

von Economo, C. (2009). Cellular Structure of the Human Cerebral Cortex. Basel: S. Karger AG.

Vyleta, N. P., & Snyder, J. S. (2021). Prolonged development of long-term potentiation at lateral entorhinal cortex synapses onto adult-born neurons. PloS one, 16(6), e0253642. https://doi.org/10.1371/journal.pone.0253642

Waaga, T., Agmon, H., Normand, V. A., Nagelhus, A., Gardner, R. J., Moser, M. B., Moser, E. I., & Burak, Y. (2022). Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues. Neuron, 110(11), 1843–1856.e6. https://doi.org/10.1016/j.neuron.2022.03.011

Wang, C., Chen, X., Lee, H., Deshmukh, S. S., Yoganarasimha, D., Savelli, F., & Knierim, J. J. (2018). Egocentric coding of external items in the lateral entorhinal cortex. Science (New York, N.Y.), 362(6417), 945–949. https://doi.org/10.1126/science.aau4940

Wang, C., Liu, H., Li, K., Wu, Z. Z., Wu, C., Yu, J. Y., Gong, Q., Fang, P., Wang, X. X., Duan, S. M., Wang, H., Gu, Y., Hu, J., Pan, B. X., Schmidt, M. V., Liu, Y. J., & Wang, X. D. (2020). Tactile modulation of memory and anxiety requires dentate granule cells along the dorsoventral axis. Nature communications, 11(1), 6045. https://doi.org/10.1038/s41467-020-19874-8

Wang, T., Yang, F., Wang, Z., Zhang, B., Wang, W., & Liu, F. (2021). Modularization of grid cells constrained by the pyramidal patch lattice. iScience, 24(4), 102301. https://doi.org/10.1016/j.isci.2021.102301

Wang, W., & Wang, W. (2021). Effect of reward on electrophysiological signatures of grid cell population activity in human spatial navigation. Scientific reports, 11(1), 23577. https://doi.org/10.1038/s41598-021-03124-y

Waniek N. (2020). Transition Scale-Spaces: A Computational Theory for the Discretized Entorhinal Cortex. Neural computation, 32(2), 330–394. https://doi.org/10.1162/neco_a_01255

Whitlock, J. R., Pfuhl, G., Dagslott, N., Moser, M. B., & Moser, E. I. (2012). Functional split between parietal and entorhinal cortices in the rat. Neuron, 73(4), 789–802. https://doi.org/10.1016/j.neuron.2011.12.028

Widloski, J., Marder, M. P., & Fiete, I. R. (2018). Inferring circuit mechanisms from sparse neural recording and global perturbation in grid cells. eLife, 7, e33503. https://doi.org/10.7554/eLife.33503

Wisse, L. E., Biessels, G. J., Heringa, S. M., Kuijf, H. J., Koek, D. H., Luijten, P. R., Geerlings, M. I., & Utrecht Vascular Cognitive Impairment (VCI) Study Group (2014). Hippocampal subfield volumes at 7T in early Alzheimer's disease and normal aging. Neurobiology of aging, 35(9), 2039–2045. https://doi.org/10.1016/j.neurobiolaging.2014.02.021

Witter, M. P., & Amaral, D. G. (2021). The entorhinal cortex of the monkey: VI. Organization of projections from the hippocampus, subiculum, presubiculum, and parasubiculum. The Journal of comparative neurology, 529(4), 828–852. https://doi.org/10.1002/cne.24983

Witter, M. P., Doan, T. P., Jacobsen, B., Nilssen, E. S., & Ohara, S. (2017). Architecture of the Entorhinal Cortex A Review of Entorhinal Anatomy in Rodents with Some Comparative Notes. Frontiers in systems neuroscience, 11, 46. https://doi.org/10.3389/fnsys.2017.00046

Witter, M. P., Kleven, H., & Kobro Flatmoen, A. (2017). Comparative Contemplations on the Hippocampus. Brain, behavior and evolution, 90(1), 15–24. https://doi.org/10.1159/000475703

Woźnicka, A., Malinowska, M., & Kosmal, A. (2006). Cytoarchitectonic organization of the entorhinal cortex of the canine brain. Brain research reviews, 52(2), 346–367. https://doi.org/10.1016/j.brainresrev.2006.04.008

Xu, X., Sun, Y., Holmes, T. C., & López, A. J. (2016). Noncanonical connections between the subiculum and hippocampal CA1. The Journal of comparative neurology, 524(17), 3666–3673. https://doi.org/10.1002/cne.24024

Yang, X., Yao, C., Tian, T., Li, X., Yan, H., Wu, J. et al. (2018). A novel mechanism of memory loss in Alzheimer's disease mice via the degeneration of entorhinal-CA1 synapses. Molecular psychiatry, 23(2), 199–210. https://doi.org/10.1038/mp.2016.151

Yartsev, M. M., Witter, M. P., & Ulanovsky, N. (2011). Grid cells without theta oscillations in the entorhinal cortex of bats. Nature, 479(7371), 103–107. https://doi.org/10.1038/nature10583

Ye, J., Witter, M. P., Moser, M. B., & Moser, E. I. (2018). Entorhinal fast-spiking speed cells project to the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 115(7), E1627–E1636. https://doi.org/10.1073/pnas.1720855115

Young J. K. (2020). Neurogenesis Makes a Crucial Contribution to the Neuropathology of Alzheimer's Disease. Journal of Alzheimer's disease reports, 4(1), 365–371. https://doi.org/10.3233/ADR-200218

Yu, X. T., Yu, J., Choi, A., & Takehara-Nishiuchi, K. (2021). Lateral entorhinal cortex supports the development of prefrontal network activity that bridges temporally discontiguous stimuli. Hippocampus, 31(12), 1285–1299. https://doi.org/10.1002/hipo.23389

Опубліковано
2023-03-15
Як цитувати
Медведєв , В., Черкасов, В., Васлович , В., & Цимбалюк , В. (2023). П’ять відкриттів Володимира Беца. Частина перша. Бец і острови енторінальної кори. Український науково-медичний молодіжний журнал, 136(1), 30-59. https://doi.org/10.32345/USMYJ.1(136).2023.30-59