SUMMARY. Modern neurobiology is based on the neuron doctrine, recognizing the main substrate of brain function as a network of neurons organized into numerous spatial and/or functional clusters – modules. The best-known illustration of this structural principle is Mountcastle’s concept of the columnar organization of the cortex, the emergence of which is associated with the idea of the vertical cortical cylinder by Lorente de No and a number of complementary cytoarchitectonic, electrophysiological, and neuroontogenetic data. In the proposed article, we present important cytoarchitectonic Betz’s observa-tions, which, from the perspective of modernity, il-lustrate the modular principle of brain organization. In particular, we demonstrate that Betz provided the first description of the «bundling» of cortical pyramidal neurons apical dendrites – one of the key morphological features of the brain modularity. We also demonstrate that Betz first described the entorhinal islands-another widespread example of cortex modular organization. Finally, we present Betz’s pioneering evidence regarding the clustered arrangement of giant pyramidal neurons in the primary motor cortex. In general, the list of Betz’s observations, consistent with the idea of a modular brain organization, includes a description of three cytoarchitectonic phenomena of the human cerebral cortex and the macroscopic counterpart of one of them – the entorhinal tuberosity.
Keywords: neurobiology, neuron doctrine, modular organization of the brain, cortical column, entorhinal islands, Betz cells, Volodymyr Betz
Full text and supplemented materials
Free full text: PDFReferences
Abraham, W.C., Jones, O.D., and Glanzman, D.L., Is plasticity of synapses the mechanism of long-term memory storage?, npj Sci. Learn., 2019, vol. 4, p. 9. https://doi.org/10.1038/s41539-019-0048-y
Amaral, D.G., Insausti, R., and Cowan, W.M., The entorhinal cortex of the monkey: I. Cytoarchitectonic organization, J. Comp. Neurol., 1987, vol. 264, no. 3, pp. 326–355. https://doi.org/10.1002/cne.902640305
Andersen, R.A. and Vernon, B., Mountcastle (1918-2015), Curr. Biol., 2015, vol. 25, no. 8, pp. R310–R313. https://doi.org/10.1016/j.cub.2015.02.039
Azevedo, E.P., Pomeranz, L., Cheng, J., Schneeberger, M., Vaughan, R., Stern, S.A., Tan, B., Doerig, K., Greengard, P., and Friedman, J.M., A role of Drd2 hippocampal neurons in context-dependent food intake, Neuron, 2019, vol. 102, no. 4, pp. 873–886.e5. https://doi.org/10.1016/j.neuron.2019.03.011
Baratham, V.L., Dougherty, M.E., Hermiz, J., Ledochowitsch, P., Maharbiz, M.M., and Bouchard, K.E., Columnar localization and laminar origin of cortical surface electrical potentials, J. Neurosci., 2022, vol. 42, no. 18, pp. 3733–3748. https://doi.org/10.1523/JNEUROSCI.1787-21.2022
Barbas, H., Zikopoulos, B., and John, Y.J., The inevitable inequality of cortical columns, Front. Syst. Neurosci., 2022, vol. 16, p. 921468. https://doi.org/10.3389/fnsys.2022.921468
Barwich, A.S., The value of failure in science: The story of grandmother cells in neuroscience, Front. Neurosci., 2019, vol. 13, p. 1121. https://doi.org/10.3389/fnins.2019.01121
Beall, M.J. and Lewis, D.A., Heterogeneity of layer II neurons in human entorhinal cortex, J. Comp. Neurol., 1992, vol. 321, no. 2, pp. 241–266, fig. 5 A, 6 A. https://doi.org/10.1002/cne.903210206
Bellmund, J.L., Deuker, L., and Doeller, C.F., Mapping sequence structure in the human lateral entorhinal cortex, Elife, 2019, vol. 8, p. e45333. https://doi.org/10.7554/eLife.45333
Bellmund, J., Polti, I., and Doeller, C.F., Sequence memory in the hippocampal-entorhinal region, J. Cognit. Neurosci., 2020, vol. 32, no. 11, pp. 2056–2070. https://doi.org/10.1162/jocn_a_01592
Betz, W., Die Untersuchungsmethode des Centralnerven-Systems des Menschen. Archiv für Mikroskopische Anatomie, Herausgegeben von Max Schultze, Bonn: Verlag von Max Cohen und Sohn, 1873, vol. IX, pp. 101–117. https://www.biodiversitylibrary.org/item/47676#page/7/mode/1up.
Betz, W., Anatomischer Nachweis zweier Gehirncentra, Centralbl. Med. Wiss., 1874, vol. 12, no. 37, pp. 578–580; vol. 12, no. 38, pp. 595–599. https://books.google.com.ua/books?id=a8ADAAAAYAAJ&redir_esc=y
Betz, W., Ueber die feinere Struktur der Gehirnrinde des Menschen, Centralbl. Med. Wiss., 1881, vol. 19, no. 11, pp. 193–195; vol. 19, no. 12, pp. 209–213; vol. 19, no. 13, pp. 231–233. https://archive.org/details/bub_gb_acADAAAAYAAJ/page/192/mode/2up.
Betz, V.A., On the details of the human cerebral cortex structure: A preliminary report, Zap. Kíevskоgo O-va. Estestvoispytat., 1882, vol. 6, no. 2, pp. 165–176. http://ukr.catalogue.nlu.org.ua/?page=2&arg2=записки киевского
Bitzenhofer, S.H., Westeinde, E.A., Zhang, H.B., and Isaacson, J.S., Rapid odor processing by layer 2 subcircuits in lateral entorhinal cortex, Elife, 2022, vol. 11, p. e75065. https://doi.org/10.7554/eLife.75065
Bliss, T. and Collingridge, G.L., Persistent memories of long-term potentiation and the N-methyl-d-aspartate receptor, Brain Neurosci. Adv., 2019, vol. 3, p. 2398212819848213. https://doi.org/10.1177/2398212819848213
Braak, H., Zur pigmentarchitektonik der grosshirnrinde des menschen. I. Regio entorhinalis, Z. Zellforsch. Mikrosk. Anat., 1948, 1972, vol. 127, no. 3, pp. 407–438, fig. 1 E, F. https://doi.org/10.1007/BF00306883
Braden, B.B. and Riecken, C., Thinning faster? Age-related cortical thickness differences in adults with autism spectrum disorder, Res. Autism Spectr. Disord., 2019, vol. 64, pp. 31–38. https://doi.org/10.1016/j.rasd.2019.03.005
Butti, C. and Hof, P.R., The insular cortex: a comparative perspective, Brain Struct. Funct., 2010, vol. 214, nos. 5–6, pp. 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., and Hof, P.R., The cerebral cortex of the pygmy hippopotamus, Hexaprotodon liberiensis (Cetartiodactyla, Hippopotamidae): MRI, cytoarchitecture, and neuronal morphology, Anat. Rec., 2014, vol. 297, no. 4, pp. 670–700. https://doi.org/10.1002/ar.22875
Buxhoeveden, D.P. and Casanova, M.F., The minicolumn and evolution of the brain, Brain Behav. Evol., 2002a, vol. 60, no. 3, pp. 125–151. https://doi.org/10.1159/000065935
Buxhoeveden, D.P. and Casanova, M.F., The minicolumn hypothesis in neuroscience, Brain, 2002, vol. 125, no. 5, pp. 935–951. https://doi.org/10.1093/brain/awf110
Buxhoeveden, D.P., Minicolumn size and human cortex, Prog. Brain Res., 2012, vol. 195, pp. 219–235. https://doi.org/10.1016/B978-0-444-53860-4.00010-6
Casanova, M.F. and Casanova, E.L., The modular organization of the cerebral cortex: Evolutionary significance and possible links to neurodevelopmental conditions, J. Comp. Neurol., 2019, vol. 527, no. 10, pp. 1720–1730. https://doi.org/10.1002/cne.24554
Crandall, S.R., Patrick, S.L., Cruikshank, S.J., and Connors, B.W., Infrabarrels are layer 6 circuit modules in the barrel cortex that link long-range inputs and outputs, Cell Rep., 2017, vol. 21, no. 11, pp. 3065–3078. https://doi.org/10.1016/j.celrep.2017.11.049
da Costa, N.M. and Martin, K.A., Whose cortical column would that be?, Front. Neuroanat., 2010, vol. 4, p. 16. https://doi.org/10.3389/fnana.2010.00016
Dang, R., Zhou, Y., Zhang, Y., Liu, D., Wu, M., Liu, A., Jia, Z., and Xie, W., Regulation of social memory by lateral entorhinal cortical projection to dorsal hippocampal CA2, Neurosci. Bull., 2022, vol. 38, no. 3, pp. 318–322. https://doi.org/10.1007/s12264-021-00813-6
Ding, S.L., Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent, J. Comp. Neurol., 2013, vol. 521, no. 18, pp. 4145–4162. https://doi.org/10.1002/cne.23416
Doan, T.P., Lagartos-Donate, M.J., Nilssen, E.S., Ohara, S., and Witter, M.P., Convergent projections from perirhinal and postrhinal cortices suggest a multisensory nature of lateral, but not medial, entorhinal cortex, Cell Rep., 2019, vol. 29, no. 3, pp. 617–627.e7. https://doi.org/10.1016/j.celrep.2019.09.005
Dorian, C.C., Taxidis, J., and Golshani, P., Non-spatial hippocampal behavioral timescale synaptic plasticity during working memory is gated by entorhinal inputs, bioRxiv, 2024. (Preprint). https://doi.org/10.1101/2024.08.27.609983
Dringenberg, H.C., The history of long-term potentiation as a memory mechanism: Controversies, confirmation, and some lessons to remember, Hippocampus, 2020, vol. 30, no. 9, pp. 987–1012. https://doi.org/10.1002/hipo.23213
East, B.S., Jr Brady, L.R., and Quinn, J.J., Differential effects of lateral and medial entorhinal cortex lesions on trace, delay and contextual fear memories, Brain Sci., 2021, vol. 12, no. 1, p. 34. https://doi.org/10.3390/brainsci12010034
Ferbinteanu, J., Holsinger, R.M., and McDonald, R.J., Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context, Behav. Brain Res., 1999, vol. 101, no. 1, pp. 65–84. https://doi.org/10.1016/s0166-4328(98)00144-2
Fifková, E., The effect of monocular deprivation on the synaptic contacts of the visual cortex, J. Neurobiol., 1969, vol. 1, no. 3, pp. 285–294. https://doi.org/10.1002/neu.480010304
Fleischhauer, K., Petsche, H., and Wittkowski, W., Vertical bundles of dendrites in the neocortex, Z. Anat. Entwicklungsgesch., 1972, vol. 136, no. 2, pp. 213–223. https://doi.org/10.1007/BF00519179
Fyhn, M., Hafting, T., Treves, A., Moser, M.B., and Moser, E.I., Hippocampal remapping and grid realignment in entorhinal cortex, Nature, 2007, vol. 446, no. 7132, pp. 190–194. https://doi.org/10.1038/nature05601
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., and Maione, S., Long-term neuropathic pain behaviors correlate with synaptic plasticity and limbic circuit alteration: a comparative observational study in mice, Pain, 2022, vol. 163, no. 8, pp. 1590–1602. https://doi.org/10.1097/j.pain.0000000000002549
Hafting, T., Fyhn, M., Molden, S., Moser, M.B., and Moser, E.I., Microstructure of a spatial map in the entorhinal cortex, Nature, 2005, vol. 436, no. 7052, pp. 801–806. https://doi.org/10.1038/nature03721
Haueis, P., Meeting the brain on its own terms, Front. Hum. Neurosci., 2014, vol. 8, p. 815. https://doi.org/10.3389/fnhum.2014.00815
Haueis, P., The life of the cortical column: opening the domain of functional architecture of the cortex (1955–1981), Hist. Philos. Life Sci., 2016, vol. 38, no. 3, p. 2. https://doi.org/10.1007/s40656-016-0103-4
Haueis, P., The death of the cortical column? Patchwork structure and conceptual retirement in neuroscientific practice, Stud. Hist. Philos. Sci., 2021, vol. 85, pp. 101–113. https://doi.org/10.1016/j.shpsa.2020.09.010
Hawkins, J., Ahmad, S., and Cui, Y., A theory of how columns in the neocortex enable learning the structure of the world, Front. Neural Circuits, 2017, vol. 11, p. 81. https://doi.org/10.3389/fncir.2017.00081
Heinsen, H., Henn, R., Eisenmenger, W., Götz, M., Bohl, J., Bethke, B., Lockemann, U., and Püschel, K., Quantitative investigations on the human entorhinal area: left-right asymmetry and age-related changes, Anat. Embryol., 1994, vol. 190, no. 2, pp. 181–194. https://doi.org/10.1007/BF00193414
Hevner, R.F. and Wong-Riley, M.T., Entorhinal cortex of the human, monkey, and rat: Metabolic map as revealed by cytochrome oxidase, J. Comp. Neurol., 1992, vol. 326, no. 3, pp. 451–469. https://doi.org/10.1002/cne.903260310
Hisey, E., Purkey, A., Gao, Y., Hossain, K., Soderling, S.H., and Ressler, K.J., A ventromedial prefrontal-to-lateral entorhinal cortex pathway modulates the gain of behavioral responding during threat, Biol. Psychiatry, 2023, vol. 94, no. 3, pp. 239–248. https://doi.org/10.1016/j.biopsych.2023.01.009
Hof, P.R. and Van der Gucht, E., Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae), Anat. Rec., 2007, vol. 290, no. 1, pp. 1–31. https://doi.org/10.1002/ar.20407
Horton, J.C. and Adams, D.L., The cortical column: a structure without a function, Philos. Trans. R. Soc., B, 2005, vol. 360, no. 1456, pp. 837–862. https://doi.org/10.1098/rstb.2005.1623
Hosoya, T., The basic repeating modules of the cerebral cortical circuit, Proc. Jpn. Acad., Ser. B, 2019, vol. 95, no. 7, pp. 303–311. https://doi.org/10.2183/pjab.95.022
Huang, X., Schlesiger, M.I., Barriuso-Ortega, I., Leibold, C., MacLaren, D.A.A., Bieber, N., and Monyer, H., Distinct spatial maps and multiple object codes in the lateral entorhinal cortex, Neuron, 2023, vol. 111, no. 19, pp. 3068–3083.e7. https://doi.org/10.1016/j.neuron.2023.06.020
Innocenti, G.M. and Vercelli, A., Dendritic bundles, minicolumns, columns, and cortical output units, Front. Neuroanat., 2010, vol. 4, p. 11. https://doi.org/10.3389/neuro.05.011.2010
Insausti, R. and Amaral, D.G., Hippocampal formation, in The Human Nervous System, Mai, J. and Paxinos, G., Eds., Elsevier: Academic, 2012, pp. 896–942. https://doi.org/10.1016/B978-0-12-374236-0.10024-0
Insausti, R., Tuñón, T., Sobreviela, T., Insausti, A.M., and Gonzalo, L.M., The human entorhinal cortex: A cytoarchitectonic analysis, J. Comp. Neurol., 1995, vol. 355, no. 2, pp. 171–198. https://doi.org/10.1002/cne.903550203
Insausti, R., Muñoz-López, M., Insausti, A.M., and Artacho-Pérula, E., The human periallocortex: layer pattern in presubiculum, parasubiculum and entorhinal cortex. A review, Front. Neuroanat., 2017, vol. 11, p. 84. https://doi.org/10.3389/fnana.2017.00084
Issa, J.B., Radvansky, B.A., Xuan, F., and Dombeck, D.A., Lateral entorhinal cortex subpopulations represent experiential epochs surrounding reward, Nat. Neurosci., 2024, vol. 27, no. 3, pp. 536–546. https://doi.org/10.1038/s41593-023-01557-4
Jones, E.G., Microcolumns in the cerebral cortex, Proc. Natl. Acad. Sci. U. S. A., 2000, vol. 97, no. 10, pp. 5019–5021. https://doi.org/10.1073/pnas.97.10.5019
Jun, H., Lee, J.Y., Bleza, N.R., Ichii, A., Donohue, J.D., and Igarashi, K.M., Prefrontal and lateral entorhinal neurons co-dependently learn item-outcome rules, Nature, 2024, vol. 633, no. 8031, pp. 864–871. https://doi.org/10.1038/s41586-024-07868-1
Kobro-Flatmoen, A. and Witter, M.P., Neuronal chemo-architecture of the entorhinal cortex: A comparative review, Eur. J. Neurosci., 2019, vol. 50, no. 10, pp. 3627–3662. https://doi.org/10.1111/ejn.14511
Kobro-Flatmoen, A., Lagartos-Donate, M.J., Aman, Y., Edison, P., Witter, M.P., and Fang, E.F., Re-emphasizing early Alzheimer’s disease pathology starting in select entorhinal neurons, with a special focus on mitophagy, Ageing Res. Rev., 2021, vol. 67, p. 101307. https://doi.org/10.1016/j.arr.2021.101307
Koskinas, G.N., Appendix. An outline of cytoarchitectonics of the adult human cerebral cortex, in Cellular Structure of the Human Cerebral Cortex, Triarhou, L.C., Ed., Basel: S. Karger AG, 2009, 245 p., P. 209.
Kringel, R., Song, L., Xu, X., Bitzenhofer, S.H., and Hanganu-Opatz, I.L., Layer-specific impairment in the developing lateral entorhinal cortex of immune-challenged Disc1+/– mice, J. Physiol., 2023, vol. 601, no. 4, pp. 847–857. https://doi.org/10.1113/JP283896
Lara-González, E., Padilla-Orozco, M., Fuentes-Serrano, A., Bargas, J., and Duhne, M., Translational neuronal ensembles: Neuronal microcircuits in psychology, physiology, pharmacology and pathology, Front. Syst. Neurosci., 2022, vol. 16, p. 979680. https://doi.org/10.3389/fnsys.2022.979680
Larriva-Sahd, J.A., Some predictions of Rafael Lorente de Nó 80 years later, Front. Neuroanat., 2014, vol. 8, p. 147. https://doi.org/10.3389/fnana.2014.00147
Larsen, N.Y., Li, X., Tan, X., Ji, G., Lin, J., Rajkowska, G., Møller, J., Vihrs, N., Sporring, J., Sun, F., and Nyengaard, J.R., Cellular 3D-reconstruction and analysis in the human cerebral cortex using automatic serial sections, Commun. Biol., 2021, vol. 4, no. 1, p. 1030. https://doi.org/10.1038/s42003-021-02548-6
Lee, W.J., Brown, J.A., Kim, H.R., La Joie, R., Cho, H., Lyoo, C.H., Rabinovici, G.D., Seong, J.K., and Seeley, W.W., Alzheimer’s disease neuroimaging initiative, regional Aβ-tau interactions promote onset and acceleration of Alzheimer’s disease tau spreading, Neuron, 2022, vol. 110, no. 12, pp. 1932–1943.e5. https://doi.org/10.1016/j.neuron.2022.03.034
Leise, E.M., Modular construction of nervous systems: a basic principle of design for invertebrates and vertebrates, Brain Res. Brain Res. Rev., 1990, vol. 15, no. 1, pp. 1–23. https://doi.org/10.1016/0165-0173(90)90009-d
Liu, P., Gao, C., Wu, J., Wu, T., Zhang, Y., Liu, C., Sun, C., and Li, A., Negative valence encoding in the lateral entorhinal cortex during aversive olfactory learning, Cell Rep., 2023, vol. 42, no. 10, p. 113204. https://doi.org/10.1016/j.celrep.2023.113204
Lopez-Rojas, J., de Solis, C.A., Leroy, F., Kandel, E.R., and Siegelbaum, S.A., A direct lateral entorhinal cortex to hippocampal CA2 circuit conveys social information required for social memory, Neuron, 2022, vol. 110, no. 9, pp. 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., and Guan, J.S., Acquiring new memories in neocortex of hippocampal-lesioned mice, Nat. Commun., 2022, vol. 13, no. 1, p. 1601. https://doi.org/10.1038/s41467-022-29208-5
Mahnke, L., Atucha, E., Pina-Fernàndez, E., Kitsukawa, T., and Sauvage, M.M., Lesion of the hippocampus selectively enhances LEC’s activity during recognition memory based on familiarity, Sci. Rep., 2021, vol. 11, no. 1, p. 19085. https://doi.org/10.1038/s41598-021-98509-4
Martin, K. and Vernon, B., Mountcastle (1918-2015), Nature, 2015, vol. 518, no. 7539, p. 304. https://doi.org/10.1038/518304a
Medvediev, V., Cherkasov, V., Vaslovych, V., and Tsymbaliuk, V., Five discoveries of Volodymyr Betz. Part one. Betz and the islands of entorhinal cortex, Ukr. Sci. Med. Youth J., 2023, vol. 136, no. 1, pp. 30–59. https://doi.org/10.32345/USMYJ.1(136).2023.30-59
Medvediev, V.V., Cherkasov, V.G., Marushchenko, M.O., Vaslovych, V.V., and Tsymbaliuk, V.I., Giant fusiform cells of the brain: discovery, identification, and probable functions, Cytol. Genet., 2024, vol. 58, pp. 411–427. https://doi.org/10.3103/S0095452724050098
Merlo, S.A., Belluscio, M.A., Pedreira, M.E., and Merlo, E., Memory persistence: from fundamental mechanisms to translational opportunities, Transl. Psychiatr., 2024, vol. 14, no. 1, p. 98. https://doi.org/10.1038/s41398-024-02808-z
Meyer, G., Forms and spatial arrangement of neurons in the primary motor cortex of man, J. Comp. Neurol., 1987, vol. 262, no. 3, pp. 402–428, fig. 2. https://doi.org/10.1002/cne.902620306
Millhouse, O.E., Granule cells of the olfactory tubercle and the question of the islands of Calleja, J. Comp. Neurol., 1987, vol. 265, no. 1, pp. 1–24. https://doi.org/10.1002/cne.902650102
Montchal, M.E., Reagh, Z.M., and Yassa, M.A., Precise temporal memories are supported by the lateral entorhinal cortex in humans, Nat. Neurosci., 2019, vol. 22, no. 2, pp. 284–288. https://doi.org/10.1038/s41593-018-0303-1
Moser, E.I., Moser, M.B., and McNaughton, B.L., Spatial representation in the hippocampal formation: a history, Nat. Neurosci., 2017, vol. 20, no. 11, pp. 1448–1464. https://doi.org/10.1038/nn.4653
Mountcastle, V.B., Modality and topographic properties of single neurons of cat’s somatic sensory cortex, J. Neurophysiol., 1957, vol. 20, no. 4, pp. 408–434. https://doi.org/10.1152/jn.1957.20.4.408
Mountcastle, V.B., The columnar organization of the neocortex, Brain, 1997, vol. 120, no. 4, pp. 701–722. https://doi.org/10.1093/brain/120.4.701
Mountcastle, V.B., Introduction. Computation in cortical columns, Cereb. Cortex, 2003, vol. 13, no. 1, pp. 2–4. https://doi.org/10.1093/cercor/13.1.2
Naumann, R.K., Ray, S., Prokop, S., Las, L., Heppner, F.L., and Brecht, M., Conserved size and periodicity of pyramidal patches in layer 2 of medial/caudal entorhinal cortex, J. Comp. Neurol., 2016, vol. 524, no. 4, pp. 783–806, fig. 8 B. https://doi.org/10.1002/cne.23865
Naumann, R.K., Preston-Ferrer, P., Brecht, M., and Burgalossi, A., Structural modularity and grid activity in the medial entorhinal cortex, J. Neurophysiol., 2018, vol. 119, no. 6, pp. 2129–2144. https://doi.org/10.1152/jn.00574.2017
Navarro Schröder, T., Haak, K.V., Zaragoza Jimenez, N.I., Beckmann, C.F., and Doeller, C.F., Functional topography of the human entorhinal cortex, Elife, 2015, vol. 4, p. e06738. https://doi.org/10.7554/eLife.06738
Nilssen, E.S., Doan, T.P., Nigro, M.J., Ohara, S., and Witter, M.P., Neurons and networks in the entorhinal cortex: A reappraisal of the lateral and medial entorhinal subdivisions mediating parallel cortical pathways, Hippocampus, 2019, vol. 29, no. 12, pp. 1238–1254. https://doi.org/10.1002/hipo.23145
Ohara, S., Yoshino, R., Kimura, K., Kawamura, T., Tanabe, S., Zheng, A., Nakamura, S., Inoue, K.I., Takada, M., Tsutsui, K.I., and Witter, M.P., Laminar organization of the entorhinal cortex in macaque monkeys based on cell-type-specific markers and connectivity, Front. Neural Circuits, 2021, vol. 15, p. 790116. https://doi.org/10.3389/fncir.2021.790116
Olajide, O.J., Suvanto, M.E., and Chapman, C.A., Molecular mechanisms of neurodegeneration in the entorhinal cortex that underlie its selective vulnerability during the pathogenesis of Alzheimer’s disease, Biol. Open, 2021, vol. 10, no. 1, p. bio056796. https://doi.org/10.1242/bio.056796
Opris, I. and Casanova, M.F., Prefrontal cortical minicolumn: from executive control to disrupted cognitive processing, Brain, 2014, vol. 137, no. 7, pp. 1863–1875. https://doi.org/10.1093/brain/awt359
Opris, I., Chang, S., and Noga, B.R., what is the evidence for inter-laminar integration in a prefrontal cortical minicolumn?, Front. Neuroanat., 2017, vol. 11, p. 116. https://doi.org/10.3389/fnana.2017.00116
Persson, B.M., Ambrozova, V., Duncan, S., Wood, E.R., O’Connor, A.R., and Ainge, J.A., Lateral entorhinal cortex lesions impair odor-context associative memory in male rats, J. Neurosci. Res., 2022, vol. 100, no. 4, pp. 1030–1046. https://doi.org/10.1002/jnr.25027
Peters, A. and Walsh, T.M., A study of the organization of apical dendrites in the somatic sensory cortex of the rat, J. Comp. Neurol., 1972, vol. 144, no. 3. pp. 253–268. https://doi.org/10.1002/cne.901440302
Pilkiw, M., Jarovi, J., and Takehara-Nishiuchi, K., Lateral entorhinal cortex suppresses drift in cortical memory representations, J. Neurosci., 2022, vol. 42, no. 6, pp. 1104–1118. https://doi.org/10.1523/JNEUROSCI.1439-21.2021
Raghanti, M.A., Spurlock, L.B., Treichler, F.R., Weigel, S.E., Stimmelmayr, R., Butti, C., Thewissen, J.G., and Hof, P.R., An analysis of von Economo neurons in the cerebral cortex of cetaceans, artiodactyls, and perissodactyls, Brain Struct. Funct., 2015, vol. 220, no. 4, pp. 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.G.M., Butti, C., and Hof, P.R., A Comparison of the cortical structure of the bowhead whale (Balaena mysticetus), a basal mysticete, with other cetaceans, Anat. Rec., 2019, vol. 302, no. 5, pp. 745–760. https://doi.org/10.1002/ar.23991
Rakic, P., Specification of cerebral cortical areas, Science, 1988, vol. 241, no. 4862, pp. 170–176. https://doi.org/10.1126/science.3291116
Rakic, P., Confusing cortical columns, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, no. 34, pp. 12099–12100. https://doi.org/10.1073/pnas.0807271105
Rakic, P., Evolution of the neocortex: a perspective from developmental biology, Nat. Rev. Neurosci., 2009, vol. 10, no. 10, pp. 724–735. https://doi.org/10.1038/nrn2719
Rakic, P., Ayoub, A.E., Breunig, J.J., and Dominguez, M.H., Decision by division: making cortical maps, Trends Neurosci., 2009, vol. 32, no. 5, pp. 291–301. https://doi.org/10.1016/j.tins.2009.01.007
Ramón y Cajal, S., Studies on the human cerebral cortex II: structure of the motor cortex of man and higher mammals, in Cajal on the Cerebral Cortex: An Annotated Translation of the Complete Writings, DeFelipe, J. and Jones, E.G., Eds., New York: Oxford Univ. Press, 1899–1900 , P. 190.
Ramón y Cajal, S., Studies on the human cerebral cortex IV: structure of the olfactory cerebral cortex of man and mammals, in Cajal on the Cerebral Cortex: An Annotated Translation of the Complete Writings, DeFelipe, J. and Jones, E.G., Eds., New York: Oxford Univ. Press, 1901–1902, P. 294–295, 301 (fig. 15).
Robertson, J.M., The gliocentric brain, Int. J. Mol. Sci., 2018, vol. 19, no. 10, p. 3033. https://doi.org/10.3390/ijms19103033
Rockland, K.S., Five points on columns, Front. Neuroanat., 2010, vol. 4, p. 22. https://doi.org/10.3389/fnana.2010.00022
Rockland, K.S. and Ichinohe, N., Some thoughts on cortical minicolumns, Exp. Brain Res., 2004, vol. 158, no. 3, pp. 265–277. https://doi.org/10.1007/s00221-004-2024-9
Rodríguez, J.J. and Verkhratsky, A., Rafael Lorente de Nó, The pioneer of physiologycal neuroanatomy, The Federation of European Physiological Societies, Famous European Physiologists, 1902—1990, pp. 1–6. https://www.feps.org/yuklemeler/famous_european_physiologists/RafaelLorentedeNo.pdf
Roe, A.W., Columnar connectome: toward a mathematics of brain function, Network Neurosci., 2019, vol. 3, no. 3, pp. 779–791. https://doi.org/10.1162/netn_a_00088
Roy, A., The theory of localist representation and of a purely abstract cognitive system: The evidence from cortical columns, category cells, and multisensory neurons, Front. Psychol., 2017, vol. 8, p. 186. https://doi.org/10.3389/fpsyg.2017.00186
Scheibel, M.E., Davies, T.L., Lindsay, R.D., and Scheibel, A.B., Basilar dendrite bundles of giant pyramidal cells, Exp. Neurol., 1974, vol. 42, no. 2, pp. 307–319. https://doi.org/10.1016/0014-4886(74)90028-4
Simic, G., Bexheti, S., Kelovic, Z., Kos, M., Grbic, K., Hof, P.R., and Kostovic, I., Hemispheric asymmetry, modular variability and age-related changes in the human entorhinal cortex, Neuroscience, 2005, vol. 130, no. 4, pp. 911–925. https://doi.org/10.1016/j.neuroscience.2004.09.040
Snyder, S.H. and Vernon, B., Mountcastle 1918-2015, Nat. Neurosci., 2015, vol. 18, no. 3, p. 318. https://doi.org/10.1038/nn.3958
Solodkin, A. and Van Hoesen, G. W., Entorhinal cortex modules of the human brain. J Comp Neurol., 1996, vol. 365, no. 4, pp. 610–617, P. 620. https://doi.org/10.1002/(SICI)1096-9861(19960219) 365:4<610::AID-CNE8>3.0.CO;2-7
Stephan, H., Allocortex, Berlin: Springer-Verlag, 1975. P. 642, 666.
Suzuki, W.A. and Porteros, A., Distribution of calbindin D-28k in the entorhinal, perirhinal, and parahippocampal cortices of the macaque monkey, J. Comp. Neurol., 2002, vol. 451, no. 4, pp. 392–412, fig. 6 B, fig. 8. https://doi.org/10.1002/cne.10370
Szentágothai, J., The ‘module-concept’ in cerebral cortex architecture, Brain Res., 1975, vol. 95, nos. 2–3, pp. 475–496. https://doi.org/10.1016/0006-8993(75)90122-5
Takehara-Nishiuchi, K., Neuronal code for episodic time in the lateral entorhinal cortex, Front. Integr. Neurosci., 2022, vol. 16, p. 899412. https://doi.org/10.3389/fnint.2022.899412
Telnykh, A., Nuidel, I., Shemagina, O., and Yakhno, V., A biomorphic model of cortical column for content-based image retrieval, Entropy, 2021, vol. 23, no. 11, p. 1458. https://doi.org/10.3390/e23111458
Tozzi, F., Guglielmo, S., Paraciani, C., van den Oever, M.C., Mainardi, M., Cattaneo, A., and Origlia, N., Involvement of a lateral entorhinal cortex engram in episodic-like memory recall, Cell Rep., 2024, vol. 43, no. 10, p. 114795. https://doi.org/10.1016/j.celrep.2024.114795
Tran, T.T., Speck, C.L., Gallagher, M., and Bakker, A., Lateral entorhinal cortex dysfunction in amnestic mild cognitive impairment, Neurobiol. Aging, 2022, vol. 112, pp. 151–160. https://doi.org/10.1016/j.neurobiolaging.2021.12.008
Tsao, A., Sugar, J., Lu, L., Wang, C., Knierim, J.J., Moser, M.B., and Moser, E.I., Integrating time from experience in the lateral entorhinal cortex, Nature, 2018, vol. 561, no. 7721, pp. 57–62. https://doi.org/10.1038/s41586-018-0459-6
Van Hoesen, G.W., Augustinack, J.C., Dierking, J., Redman, S.J., and Thangavel, R., The parahippocampal gyrus in Alzheimer’s disease. Clinical and preclinical neuroanatomical correlates, Ann. N. Y. Acad. Sci., 2000, vol. 911, pp. 254–274. https://doi.org/10.1111/j.1749-6632.2000.tb06731.x
Vandrey, B., Garden, D.L.F., Ambrozova, V., McClure, C., Nolan, M.F., and Ainge, J.A., Fan cells in layer 2 of the lateral entorhinal cortex are critical for episodic-like memory, Curr. Biol., 2020, vol. 30, no. 1, pp. 169–175.e5. https://doi.org/10.1016/j.cub.2019.11.027
Vandrey, B., Armstrong, J., Brown, C.M., Garden, D.L.F., and Nolan, M.F., Fan cells in lateral entorhinal cortex directly influence medial entorhinal cortex through synaptic connections in layer 1, Elife, 2022, vol. 11, p. e83008. https://doi.org/10.7554/eLife.83008
von Bonin, G. and Mehler, W.R., On columnar arrangement of nerve cells in cerebral cortex, Brain Res., 1971, vol. 27, no. 1, pp. 1–9. https://doi.org/10.1016/0006-8993(71)90367-2
von Economo, C., Introduction, in Cellular Structure of the Human Cerebral Cortex, Triarhou, L.C., Ed., Basel: S. Karger AG, 2009a, p. 2.
von Economo, C., Hippocampal (Inferior Limbic) Lobe. Hippocampal gyrus, dentate gyrus and uncus, in Cellular Structure of the Human Cerebral Cortex, Triarhou, L.C., Ed., Basel: S. Karger AG, 2009b, pp. 150–169.
Wang, C., Lee, H., Rao, G., and Knierim, J.J., Multiplexing of temporal and spatial information in the lateral entorhinal cortex, Nat. Commun., 2024, vol. 15, no. 1, p. 10533. https://doi.org/10.1038/s41467-024-54932-5
Witter, M.P., Groenewegen, H.J., Lopes da Silva, F.H., and Lohman, A.H., Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region, Prog. Neurobiol. (N. Y.), 1989, vol. 33, no. 3, pp. 161–253. https://doi.org/10.1016/0301-0082(89)90009-9
Witter, M.P., Doan, T.P., Jacobsen, B., Nilssen, E.S., and Ohara, S., Architecture of the entorhinal cortex a review of entorhinal anatomy in rodents with some comparative notes, Front. Syst. Neurosci., 2017a, vol. 11, p. 46. https://doi.org/10.3389/fnsys.2017.00046
Witter, M.P., Kleven, H., and Kobro Flatmoen, A., Comparative contemplations on the hippocampus, Brain Behav. Evol., 2017b, vol. 90, no. 1, pp. 15–24. https://doi.org/10.1159/000475703
Woźnicka, A., Malinowska, M., and Kosmal, A., Cytoarchitectonic organization of the entorhinal cortex of the canine brain, Brain Res. Rev., 2006, vol. 52, no. 2, pp. 346–367. https://doi.org/10.1016/j.brainresrev.2006.04.008
Wu, T., Li, S., Du, D., Li, R., Liu, P., Yin, Z., Zhang, H., Qiao, Y., and Li, A., Olfactory-auditory sensory integration in the lateral entorhinal cortex, Prog. Neurobiol. (N. Y.), 2023, vol. 221, p. 102399. https://doi.org/10.1016/j.pneurobio.2022.102399
Xu, X., Sun, Y., Holmes, T.C., and López, A.J., Noncanonical connections between the subiculum and hippocampal CA1, J. Comp. Neurol., 2016, vol. 524, no. 17, pp. 3666–3673. https://doi.org/10.1002/cne.24024
Yu, X.T., Yu, J., Choi, A., and Takehara-Nishiuchi, K., Lateral entorhinal cortex supports the development of prefrontal network activity that bridges temporally discontiguous stimuli, Hippocampus, 2021, vol. 31, no. 12, pp. 1285–1299. https://doi.org/10.1002/hipo.23389
Yun, S., Soler, I., Tran, F.H., Haas, H.A., Shi, R., Bancroft, G.L., Suarez, M., de Santis, C.R., Reynolds, R.P., and Eisch, A.J., Behavioral pattern separation and cognitive flexibility are enhanced in a mouse model of increased lateral entorhinal cortex-dentate gyrus circuit activity, Front. Behav. Neurosci., 2023, vol. 17, p. 1151877. https://doi.org/10.3389/fnbeh.2023.1151877
Yuste, R., From the neuron doctrine to neural networks, Nat. Rev. Neurosci., 2015, vol. 16, no. 8, pp. 487–497. https://doi.org/10.1038/nrn3962