In search of common developmental and evolutionary origin of the claustrum and subplate.
claustrum
development
dorsal endopiriform nucleus
evolution
insular cortex
lateral amygdala
layer6b
subplate
Journal
The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041
Informations de publication
Date de publication:
01 12 2020
01 12 2020
Historique:
received:
31
01
2020
revised:
01
04
2020
accepted:
02
04
2020
pubmed:
9
4
2020
medline:
12
11
2021
entrez:
9
4
2020
Statut:
ppublish
Résumé
The human claustrum, a major hub of widespread neocortical connections, is a thin, bilateral sheet of gray matter located between the insular cortex and the striatum. The subplate is a largely transient cortical structure that contains some of the earliest generated neurons of the cerebral cortex and has important developmental functions to establish intra- and extracortical connections. In human and macaque some subplate cells undergo regulated cell death, but some remain as interstitial white matter cells. In mouse and rat brains a compact layer is formed, Layer 6b, and it remains underneath the cortex, adjacent to the white matter. Whether Layer 6b in rodents is homologous to primate subplate or interstitial white matter cells is still debated. Gene expression patterns, such as those of Nurr1/Nr4a2, have suggested that the rodent subplate and the persistent subplate cells in Layer 6b and the claustrum might have similar origins. Moreover, the birthdates of the claustrum and Layer 6b are similarly precocious in mice. These observations prompted our speculations on the common developmental and evolutionary origin of the claustrum and the subplate. Here we systematically compare the currently available data on cytoarchitecture, evolutionary origin, gene expression, cell types, birthdates, neurogenesis, lineage and migration, circuit connectivity, and cell death of the neurons that contribute to the claustrum and subplate. Based on their similarities and differences we propose a partially common early evolutionary origin of the cells that become claustrum and subplate, a likely scenario that is shared in these cell populations across all amniotes.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2956-2977Subventions
Organisme : Medical Research Council
ID : MR/N026039/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/F003285/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 204651/Z/16/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0300200
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0900901
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0700377
Pays : United Kingdom
Informations de copyright
© 2020 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals, Inc.
Références
Abbie, A. (1940). Cortical lamination in the monotremata. The Journal of Comparative Neurology, 72(3), 429-467.
Aboitiz, F., Montiel, J., & García, R. (2005). Ancestry of the mammalian preplate and its derivatives: Evolutionary relicts or embryonic adaptations? Reviews in the Neurosciences, 16(4), 359-376.
Aboitiz, F. (1999). Feature article: Comparative development of the mammalian isocortex and the reptilian dorsal ventricular ridge. Evolutionary considerations. Cerebral Cortex, 9(8), 783-791. https://doi.org/10.1093/cercor/9.8.783
Allendoerfer, K., & Shatz, C. (1994). The subplate, a transient neocortical structure: Its role in the development of connections between thalamus and cortex. Annual Review of Neuroscience, 17(1), 185-218.
Anderson, S. (1997). Interneuron migration from basal forebrain to neocortex: Dependence on Dlx genes. Science, 278(5337), 474-476.
Angevine, J. B., Jr., & Sidman, R. L. (1961). Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature, 192, 766-768.
Arias, M., Baratta, J., Yu, J., & Robertson, R. (2002). Absence of selectivity in the loss of neurons from the developing cortical subplate of the rat. Developmental Brain Research, 139(2), 331-335.
Arimatsu, Y., Ishida, M., Kaneko, T., Ichinose, S., & Omori, A. (2003). Organization and development of corticocortical associative neurons expressing the orphan nuclear receptor Nurr1. The Journal of Comparative Neurology, 466(2), 180-196.
Ashwell, K. W., Hardman, C., & Paxinos, G. (2004). The claustrum is not missing from all monotreme brains. Brain, Behaviour and Evolution, 64(4), 223-241.
Atlan, G., Terem, A., Peretz-Rivlin, N., Groysman, M., & Citri, A. (2016). Mapping synaptic cortico-claustral connectivity in the mouse. Journal of Comparative Neurology, 525(6), 1381-1402.
Atlan, G., Terem, A., Peretz-Rivlin, N., Sehrawat, K., Gonzales, B. J., Pozner, G., … Citri, A. (2018). The claustrum supports resilience to distraction. Current Biology, 28(17), 1-11.
Baizer, J., Sherwood, C., Noonan, M., & Hof, P. R. (2014). Comparative organization of the claustrum: What does structure tell us about function? Frontiers in Systems Neuroscience, 8, https://www.ncbi.nlm.nih.gov/pubmed/25071474.
Bayer, S., & Altman, J. (1990). Development of layer I and the subplate in the rat neocortex. Experimental Neurology, 107(1), 48-62.
Bayer, L., Serafin, M., Eggermann, E., Saint-Mleux, B., Machard, D., Jones, B. E., & Mühlethaler, M. (2004). Exclusive postsynaptic action of hypocretin-orexin on sublayer 6b cortical neurons. Journal of Neuroscience, 24, 6760-6764.
Belgard, T. H., Marques, A. C., Oliver, P. L., Abaan, H. O., Sirey, T. M., Hoerder-Suabedissen, A., … Ponting, C. P. (2011). A transcriptomic atlas of mouse neocortical layers. Neuron, 71(4), 605-616.
Belgard, T. G., Montiel, J. F., Wang, W. Z., García-Moreno, F., Margulies, E. H., Ponting, C. P., & Molnár, Z. (2013). Adult pallium transcriptomes surprise in not reflecting predicted homologies across diverse chicken and mouse pallial sectors. Proceedings of the National Academy of Sciences of the United States of America, 110(32), 13150-13155.
Bickel, S., & Parvizi, J. (2019). Electrical stimulation of the human claustrum. Epilepsy & Behavior, 97, 296-303. https://doi.org/10.1016/j.yebeh.2019.03.051
Bielle, F., Griveau, A., Narboux-Nême, N., Vigneau, S., Sigrist, M., Arber, S., … Pierani, A. (2005). Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nature Neuroscience, 8(8), 1002-1012.
Binks, D., Watson, C., & Puelles, L. (2019). A re-evaluation of the anatomy of the claustrum in rodents and primates-Analyzing the effect of pallial expansion. Frontiers in Neuroanatomy, 13, https://www.ncbi.nlm.nih.gov/pubmed/25071474.
Bisconte, J.-C., & Marty, R. (1975). Analyse chronoarchitectonique du cerveau de rat par radioautographie. I. Histogenese du telencephale. Journal für Hirnforschung, 16, 55-74.
Boon, J., Clarke, E., Kessaris, N., Goffinet, A., Molnár, Z., & Hoerder-Suabedissen, A. (2019). Long-range projections from sparse populations of GABAergic neurons in murine subplate. The Journal of Comparative Neurology, 527(10), 1610-1620.
Braak, H., & Braak, E. (1982). Neuronal types in the claustrum of man. Anatomy and Embryology, 163, 447-460.
Brain Map. (2019). brain-map.org. Retrieved from http://www.brain-map.org/
Britanova, O., de Juan Romero, C., Cheung, A., Kwan, K. Y., Schwark, M., Gyorgy, A., … Tarabykin, V. (2008). Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron, 57(3), 378-392.
Brodmann, K. (1909). Vergleichende lokalisationslehre der grosshirnrinde in ihren prinzipien dargestellt auf grund des zellenbaues. Leipzig, Germany: J. A. Barth.
Butler, A. B., & Molnár, Z. (2002). Development and evolution of the collopallium in amniotes: a new hypothesis of field homology. Brain Research Bulletin, 57(3-4), 475-479.
Butler, A. B., Molnár, Z., & Manger, P. R. (2002). Apparent absence of claustrum in monotremes: Implications for forebrain evolution in amniotes. Brain, Behavior and Evolution, 60, 230-240.
Crick, F., & Koch, C. (2005). What is the function of the claustrum? Philosophical Transactions of the Royal Society B: Biological Sciences, 360, 1271-1279.
Dell, L. A., Spocter, M. A., Patzke, N., Karlson, K. AE., Alagaili, A. N., Bennett, N. C., … Manger, P. R. (2015). Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls. Journal of Chemical Neuroanatomy, 68, 61-76.
Druga, R. (2014). The structure and connections of the claustrum. In J. Smythies, L. Edelstein, & V. Ramachandran (Eds.), The claustrum: Structural, functional, and clinical neuroscience (pp. 29-84). San Diego, CA: Academic Press: Elsevier.
Duque, A., Krsnik, Z., Kostović, I., & Rakic, P. (2016). Secondary expansion of the transient subplate zone in the developing cerebrum of human and nonhuman primates. Proceedings of the National Academy of Sciences of the United States of America, 113(35), 9892-9897.
Ferrer, I., Bernet, E., Soriano, E., del Rio, T., & Fonseca, M. (1990). Naturally occuring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience, 39(2), 451-458.
Friauf, E., & Shatz, C. J. (1991). Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. Journal of Neurophysiology, 66(6), 2059-2071.
García-Moreno, F., Anderton, E., Jankowska, M., Begbie, J., Encinas, J. M., Irimia, M., & Molnár, Z. (2018). Absence of tangentially migrating glutamatergic neurons in the developing avian brain. Cell Reports, 22(1), 96-109.
González-Arnay, E., González-Gómez, M., & Meyer, G. (2017). A radial glia fascicle leads principal neurons from the pallial-subpallial boundary into the developing human insula. Frontiers in Neuroanatomy, 11, 111.
Hanganu, I. L., Okabe, A., Lessmann, V., & Luhmann, H. J. (2009). Cellular mechanisms of subplate -driven and cholinergic input-dependent network activiyt inthe neonatal rat somatosensory cortex. Cerebral Cortex, 19(1), 89-105.
Hardman, C. D., & Ashwell, K. W. S. (2012). Stereotaxic and chemoarchitectural atlas of the brain of the common marmoset (Callithrix jacchus). Boca Raton, FL: Taylor and Francis.
Higashi, S., Molnár, Z., Kurotani, T., & Toyama, K. (2002). Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording. Neuroscience, 115(4), 1231-1246.
Higashi, S., Hioki, K., Kurotani, T., Kasim, N., & Molnár, Z. (2005). Functional thalamocortical synapse reorganization from subplate to layer IV during postnatal development in the reeler-like mutant rat (shaking rat Kawasaki). The Journal of Neuroscience, 25(6), 1395-1406.
Hinds, J. W., & Angevine, J. B. (1965). Autoradiographic study of histogenesis in the area piri-formis and claustrum in the mouse. The Anatomical Record, 151, 456-457.
Hoerder-Suabedissen, A., & Molnár, Z. (2013). Molecular diveristy of early born subplate neurons. Cerebral Cortex, 23(6), 1473-1483.
Hoerder-Suabedissen, A., & Molnár, Z. (2015). Development, evolution and pathology of neocortical subplate neurones. Nature Reviews Neuroscience, 16(3), 133-146.
Hoerder-Suabedissen, A., & Molnár, Z. (2012). Morpholgy of mouse subplate cells with identified projection targets changes with age. The Journal of Comparative Neurology, 520(1), 174-185.
Hoerder-Suabedissen, A., Oeschger, F., Krishnan, M., Belgard, T., Wang, W., Lee, S., … Molnár, Z. (2013). Expression profiling of mouse subplate reveals a dynamic gene network and disease association with autism and schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 110(9), 3555-3560.
Hoerder-Suabedissen, A., Hayashi, S., Upton, L., Nolan, Z., Casas-Torremocha, D., Grant, E., … Molnár, Z. (2018). Subset of cortical layer 6b neurons selectively innervates higher order thalamic nuclei in mice. Cerebral Cortex, 28(5), 1882-1897.
Hoerder-Suabedissen, A., Wang, W. Z., Lee, S., Davies, K. E., Goffinet, A. M., Rakic, S., … Molnár, Z. (2009). Novel markers reveal subpopulatiosn of subplate neurons in the murine cerebral cortex. Cerebral Cortex, 19(8), 1738-1750.
Holl, M. (1899). Üeber die Insel des Carnivorehirns. Archiv für Anatomie und Physiologie. https://www.biodiversitylibrary.org/item/49216#page/7/mode/1up
Holmgren, N. (1925). Points of view concerning forebrain morphology in higher vertebrates. Acta Zoologica, 6(3), 413-459.
Humphrey, T. (1936). The telencephalon of the bat. The Journal of Comparative Neurology, 65(1), 603-711.
Hur, E. E., & Zaborsky, L. (2005). Vglut2 afferents to the medial prefrontal and primary somatosensory cortices: A combined retrograde tracing in situ hybridization study. Journal of Comparative Neurology, 483(3), 351-373.
Judaš, M., Sedmak, G., & Kostović, I. (2013). The significance of the subplate for evolution and developmental plasticity of the human brain. Frontiers in Human Neuroscience, 7, 423.
Judaš, M., Sestan, N., & Kostović, I. (1999). Nitrinergic neurons in the developing and adult human telencephalon: Transient and permanent patterns of expression in comparison to other mammals. Microscopy Research and Technique, 45(6), 401-419.
Judaš, M., Sedmak, G., Pletikos, M., & Jovanov-Milošević, N. (2010). Populations of subplate and interstitial neurons in fetal and adult human telencephalon. Journal of Anatomy, 217(4), 381-399.
Judaš, M. (2011). Prenatal development of human fetal telencephalon. In Fetal MRI (pp. 81-146). Berlin-New York: Springer.
Kanold, P. O., & Luhmann, H. J. (2010). The subplate and early cortical circuits. Annual Review of Neuroscience, 33, 23-48.
Kennedy, H., & Dehay, C. (2012). Self-organization and interareal networks in the primate cortex. Progress in Brain Research, 195, 341-360.
Kim, J., Matney, C. J., Roth, R. H., & Brown, S. P. (2016). Synaptic organization of the neuronal circuits of the claustrum. Journal of Neuroscience, 36(3), 773-784.
Koubeissi, M. Z., Bartolomei, F., Beltagy, A., & Picard, F. (2014). Electrical stimulation of a small brain area reversibly disrupts consciousness. Epilepsy and Behavior, 37, 32-35.
Kowiańsk, P., Dziewiątkowski, J., Kowiańska, J., & Moryś, J. (1999). Comparative anatomy of the claustrum in selected species: A morphometric analysis. Brain, Behavior and Evolution, 53(1), 44-54.
Kostović, I., Jovanov-Milošević, N., Radoš, M., Sedmak, G., Benjak, V., Kostović-Srzentić, M., … Judaš, M. (2014). Perinatal and early postnatal reorganization of the subplate and related cellular compartments in the human cerebral wall as revealed by histological and MRI approaches. Brain Structure & Function, 219(1), 231-253.
Kostović, I., & Judas, M. (2010). The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatrica, 99(8), 1119-1127.
Kostović, I., & Rakic, P. (1980). Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. Journal of Neurocytology, 9(2), 219-242.
Kostović, I., & Rakic, P. (1990). Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. Journal of Comparative Neurology, 297(3), 441-470.
Krimmel, S. R., White, M. G., Panicker, M. H., Barrett, F. S., Mathur, B. N., & Seminowicz, D. A. (2019). Resting state functional connectivity and cognitive task-related activation of the human claustrum. NeuroImage, 196, 59-67.
Li, S. B., & de Lecea, L. (2020). The hypocretin (orexin) system: From a neural circuitry perspective. Neuropharmacology, 167, 107993.
Loo, Y. T. (1931). The forebrain of the opossum Didelphis virginiana. The Journal of Comparative Neurology, 52, 1-148.
Luskin, M., & Shatz, C. (1985a). Neurogenesis of the cat's primary visual cortex. The Journal of Comparative Neurology, 242(4), 611-631.
Luskin, M., & Shatz, C. (1985b). Studies of the earliest generated cells of the cat's visual cortex: Cogeneration of subplate and marginal zones. The Journal of Neuroscience, 5(4), 1062-1075.
Marin-Padilla, M. (1978). Dual origin of the mammalian neocortex and evolution of the cortical plate. Anatomy and Embryology, 152(2), 109-126.
Marx, M., Qi, G., Hanganu-Opatz, I., Kilb, W., Luhmann, H., & Feldmeyer, D. (2017). Neocortical Layer 6B as a remnant of the subplate-A morphological comparison. Cerebral Cortex, 27(2), 1011-1026. https://doi.org/10.1093/cercor/bhv279
Mathur, B. (2014). The claustrum in review. Frontiers in Systems Neuroscience, 8, 1-11.
Mathur, B. N., Caprioli, R. M., & Deutch, A. Y. (2009). Proteomic analysis illuminates a novel structural definition of the claustrum and insula. Cerebral Cortex, 19(10), 2372-2379. https://doi.org/10.1093/cercor/bhn253
Meyer, G. (2007). Genetic control of neuronal migrations in human cortical development. Advances in Anatomy, Embryology, and Cell Biology, 189, 1-111.
Meyer, G., Castro, R., Soria, J. M., & Fairén, A. (2000). The subpial granular layer in the developing cerebral cortex of rodents. Results and Problems in Cell Differentiation, 30, 277-291.
Meyer, G., Wahle, P., Castaneyra-Perdomo, A., & Ferres-Torres, R. (1992). Morphology of neurons in the white matter of the adult human neocortex. Experimental Brain Research, 88(1), 204-212.
Molyneaux, B. J., Arlotta, P., Fame, R. M., MacDonald, J. L., MacQuarrie, K. L., & Macklis, J. D. (2009). Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. Journal of Neuroscience, 29(39), 12343-12354.
Molyneaux, B. J., Arlotta, P., Menezes, J. R., & Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nature Reviews Neuroscience, 8(6), 427-437.
Molnár, Z. (1998). Development of thalamocortical connections. Berlin, Germany: Heidelberg, Germany.
Molnár, Z. (2004). Thomas Willis (1621-1675), the founder of clinical neuroscience. Nature Reviews Neuroscience, 5(4), 329-335.
Molnár, Z. (2019). Cortical layer with no known function. The European Journal of Neuroscience, 49(7), 957-963.
Molnár, Z., & Blakemore, C. (1995). How do thalamic axons find their way to the cortex? Trends in Neurosciences, 18(9), 389-397.
Molnár, Z., & Butler, A. B. (2002). Neuronal changes during forebrain evolution in aminotes: An evolutionary developmental perspective. Progress in Brain Research, 136, 21-38.
Molnár, Z., Garel, S., López-Bendito, G., Maness, P., & Price, D. (2012). Mechanisms controlling the guidance of thalamocortical axons through the embryonic forebrain. European Journal of Neuroscience, 35(10), 1573-1585.
Molnár, Z., Knott, G. W., Blakemore, C., & Saunders, N. R. (1998). Development of thalamocortical projections in the South American gray short-tailed opossum (Monodelphis domestica). Journal of Comparative Neurology, 398(4), 491-514.
Molnár, Z., Kurotani, T., Higashi, S., Yamamoto, N., & Toyama, K. (2003). Development of functional thalamocortical synapses studied with current source-density analysis in whole forebrain slices in the rat. Brain Research Bulletin, 60(4), 355-371.
Molnár, Z., Métin, C., Stoykova, A., Tarabykin, V., Price, D. J., Francis, F., … Kennedy, H. (2006). Comparative aspects of cerebral cortical development. European Journal of Neuroscience, 23, 921-934.
Montiel, J., Wang, W., Oeschger, F., Hoerder-Suabedissen, A., Tung, W., García-Moreno, F., … Molnár, Z. (2011). Hypothesis on the dual origin of the mammalian subplate. Frontiers in Neuroanatomy, 5, 25.
Mrzljak, L., Uylings, H. B., Kostović, I., & Van Eden, C. G. (1988). Prenatal development of neurons in the human prefrontal cortex: I. A qualitative golgi study. The Journal of Comparative Neurology, 271(3), 355-386.
Narikiyo, K., Mizuguchi, R., Akima, A., Mitsui, S., Shiozaki, M., Hamanaka, H., … Yoshihara, Y. (2018). The claustrum coordinates cortical slow wave activity. bioRxiv, 1-38. https://doi.org/10.1101/286773
Narkiewicz, O., & Mamos, L. (1990). Relation of the insular claustrum to the neocortex in Insectivora. Journal für Hirnforschung, 31(5), 623-633.
Norimoto, H., Fenk, L. A., Li, H. H., Tosches, M. A., Gallego-Flores, T., Hain, D., … Laurent, G. (2020). A claustrum in reptiles and its role in slow-wave sleep. Nature, 578(7795), 413-418.
Oeschger, F. M., Wang, W. Z., Lee, S., Garcia-Moreno, F., Goffinet, A. M., Arbones, M. L., … Molnar, Z. (2011). Gene expression analysis of the embryonic subplate. Cerebral Cortex, 22(6), 1343-59.
Paolino, A., Fenlon, L. R., Suárez, R., & Richards, L. J. (2018). Transcriptional control of long-range cortical projections. Current Opinion in Neurobiology, 53, 57-65.
Patru, M. C., & Reser, D. H. (2015). A new perspective on delusional states-evidence for claustrum involvement. Frontiers in Psychiatry, 6. https://doi.org/10.3389/fpsyt.2015.00158
Paxinos, G., Watson, C., Petrides, M., Rosa, M., & Tokuno, H. (2012). The marmoset brain in stereotaxic coordinates. London: Academic Press, Elsevier.
Pearce, A., James, A. C., & Mark, R. F. (2000). Development of functional connections between thalamic fibres and the visual cortex of the wallaby revealed by current source density analysis in vivo. Journal of Comparative Neurology, 418(4), 441-456.
Pedraza, M., Hoerder-Suabedissen, A., Albert-Maestro, M. A., Molnár, Z., & De Carlos, J. A. (2014). Extracortical origin of some murine subplate cell populations. Proceedings of the National Academy of Sciences of the United States of America, 111(23), 8613-8618.
Piñon, M. C., Jethwa, A., Jacobs, E., Campagnoni, A., & Molnár, Z. (2009). Dynamic integration of subplate neurons into cortical barrel field circuitry during postnatal development in the Golli-tau-eGFP (GTE) mouse. Journal of Physiology, 587, 1903-1915.
Pirone, A., Cozzi, B., Edelstein, L., Peruffo, A., Lenzi, C., Quilici, F., … Castagna, M. (2012). Topography of Gng2- and NetrinG2-expression suggests an insular origin of the human claustrum. PLoS One, 7(9), e44745.
Price, D. J., Aslam, S., Tasker, L., & Gillies, K. (1997). Fates of the earliest generated cells in the developing murine neocortex. Journal of Comparative Neurology, 377(3), 414-422.
Puelles, L. (2014). Development and evolution of the claustrum. In J. Smythies, L. Edelstein, & V. Ramachandran (Eds.), The claustrum: Structural, functional, and clinical neuroscience (pp. 85-118). San Diego, CA: Academic Press: Elsevier.
Puelles, L. (2011). Pallio-pallial tangential migrations and growth signaling: New scenario for cortical evolution? Brain, Behavior and Evolution, 78, 108-127. https://doi.org/10.1159/000327905
Puelles, L. (2017). Comments on the updated tetrapartite pallium model in the mouse and chick, featuring a homologous claustro-insular complex. Brain, Behavior and Evolution, 90(2), 171-189.
Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J., … Rubenstein, J. L. R. (2000). Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. The Journal of Comparative Neurology, 424(3), 409-438.
Puelles, L., Ayad, A., Alonso, A., Sandoval, J. E., MartÍnez-de-la-Torre, M., Medina, L., & Ferran, J. L. (2016). Selective early expression of the orphan nuclear receptor Nr4a2 identifies the claustrum homolog in the avian mesopallium: Impact on sauropsidian/mammalian pallium comparisons. Journal of Comparative Neurology, 524(3), 665-703.
Puelles, L., Alonso, A., García-Calero, E., & Martínez-de-la-Torre, M. (2019). Concentric ring topology of mammalian cortical sectors and relevance for patterning studies. The Journal of Comparative Neurology, 527(10), 1731-1752.
Puzzolo, E., & Mallamaci, A. (2010). Cortico-cerebral histogenesis in the opossum Monodelphis domestica: generation of a hexalaminar neocortex in the absence of a basal proliferative compartment. Neural Development, 5, 8.
Ramon, Y., & Cajal, S. (1902). Studien über die Hirnrinde des Menschen. III. Heft: Die Hörrinde NB, this contains also the insular cortex (p. 63) [Translated into German by Bresler, J.] Leipzig, Barth.
Rakic, P. (1974). Neurons in rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition. Science, 183(4123), 425-427.
Real, M., Dávila, J., & Guirado, S. (2006). Immunohistochemical localization of the vesicular glutamate transporter VGLUT2 in the developing and adult mouse claustrum. Journal of Chemical Neuroanatomy, 31(3), 169-177.
Real, M. A., Dávila, J. C., & Guirado, S. (2003). Expression of calcium-binding proteins in the mouse claustrum. Journal of Chemical Neuroanatomy, 25(3), 151-160.
Reynhout, K., & Baizer, J. S. (1999). Immunoreactivity for calcium-binding proteins in the claustrum of the monkey. Anatomy and Embryology, 199(1), 75-83.
Rickmann, M., Chronwall, B. M., & Wolff, J. R. (1977). On the development of non-pyramidal neurons and axons outside the cortical plate: The early marginal zone as a pallial anlage. Anatomy and Embryology, 151(3), 285-307.
Rueda-Alaña, E., Martínez-Garay, I., Encinas, J., Molnár, Z., & García-Moreno, F. (2018). Dbx1-derived pyramidal neurons are generated locally in the developing murine neocortex. Frontiers in Neuroscience, 12, 792.
Rose, M. (1928). Die Inselrinde des Menschen und der Tiere. Journal of Psychology and Neurology, 37, 467-624.
Saito, K., Okamoto, M., Watanabe, Y., Noguchi, N., Nagasaka, A., Nishina, Y., … Miyata, T. (2019). Dorsal-to-ventral neocortical expansion is physically primed by ventral streaming of early embryonic preplate neurons. Cell Reports, 29(6), 1555-1567.
Smart, I. H., & Smart, M. (1977). The location of nuclei of different labeling intensities in auto- radiographs of the anterior forebrain of postnatal mice injected with [3H]thymidine on the eleventh and twelfth days post-conception. Journal of Anatomy, 123, 515-525.
Smart, I. H., & Smart, M. (1982). Growth patterns in the lateral wall of the mouse telencephalon: I. Autoradiographic studies of the histogenesis of the isocortex and adjacent areas. Journal of Anatomy, 134(2), 273-298.
Smith, G. (1910). The Arris and Gale lectures on some problems relating to the evolution of brain. Lancet, 175, P221-P227.
Smith, J., & Alloway, K. (2014). Interhemispheric claustral circuits coordinate sensory and motor cortical areas that regulate exploratory behaviors. Frontiers in Systems Neuroscience, 8, 93.
Smith, J., Alloway, K., Hof, P., Orman, R., Reser, D., Watakabe, A., & Watson, G. (2018). The relationship between the claustrum and endopiriform nucleus: A perspective towards consensus on cross-species homology. Jounral of Comparative Neurology, 527(2), 476-499.
Smythies, J., Edelstein, L., & Ramachandran, V. (2012). Hypotheses relating to the function of the claustrum. Frontiers in Integrative Neuroscience, 6, 53.
Sonntag, C., & Woollard, H. (1925). A monograph of Orycteropusafer. II. Nervous system, sense organs and hairs. Proceedings of the Zoological Society of London, 95(2), 1185-1235.
Suárez, R., Paolino, A., Fenlon, L. R., Morcom, L. R., Kozulin, P., Kurniawan, N. D., & Richards, L. J. (2018). A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum. Proceedings of the National Academy of Sciences of the United States of America, 115(38), 9622-9627.
Suárez-Solá, M. L., González-Delgado, F. J., Pueyo-Morlans, M., Medina-Bolívar, O. C., Hernández-Acosta, N. C., González-Gómez, M., & Meyer, G. (2009). Neurons in the white matter of the adult human neocortex. Frontiers in Neuroanatomy, 3, 7.
Supèr, H., & Uylings, H. (2001). The early differentation of the neocortex: A hypothesis on neocortical evolution. Cerebral Cortex, 11(12), 1101-1109.
Swanson, L. W. (2018). Brain maps 4.0-Structure of the rat brain: An open access atlas with global nervous system nomenclature ontology and flatmaps. The Journal of Comparative Neurology, 526(6), 935-943.
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., … Zeng, H. (2016). Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nature Neuroscience, 19(2), 335-346. https://doi.org/10.1038/nn.4216
Tasic, B., Yao, Z., Graybuck, L. T., Smith, K. A., Nguyen, T. N., Bertagnolli, D., … Zeng, H. (2018). Shared and distinct transcriptomic cell types across neocortical areas. Nature, 563(7729), 72-78.
Tigges, J., & Totada, R. (1969). A stereotaxic brain atlas of the tree shrew (Tupaia glis). Baltimore: Williams and Wilkins Company.
Torgerson, C., Irimia, A., Goh, S., & Van Horn, J. (2015). The DTI connectivity of the human claustrum. Human Brain Mapping, 36(3), 827-838.
Torgerson, C. M., Irimia, A., Goh, S. Y. M., Van Horn, J. D., (2015) The DTI connectivity of the human claustrum. Hum. Brain Mapp.36: 827-838
Tosches, M. A., Yamawaki, T. M., Naumann, R. K., Jacobi, A. A., Tushev, G., & Laurent, G. (2018). Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science, 360(6391), 881-888. https://doi.org/10.1126/science.aar4237
Valverde, F., & Santacana, M. (1994). Development of early postnatal maturation of the primary olfactory cortex. Brain Research. Developmental Brain Research, 80, 96-114.
Valverde, F., & Facal-Valverde, M. (1988). Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: A correlated Golgi and electron microscopic study. Journal of Comparative Neurology, 269(2), 168-192.
Valverde, F., Facal-Valverde, M. V., Santacana, M., & Heredia, M. (1989). Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: A correlated Golgi and autoradiographic study. The Journal of Comparative Neurology, 290, 118-140.
Valverde, F., Lopez-Mascaraque, L., Santacana, M., & De Carlos, J. A. (1995). Persistence of early-generated neurons in the rodent subplate: Assessment of cell death in neocortex during early postnatal period. Journal of Neuroscience, 15, 5014-5024.
Wang, Y., Koch, C., Luo, Q., Peng, H., & Zeng, H. (2019). Complete single neuron reconstruction reveals morphological diversity in molecularly defined claustral and cortical neuron types. BioRxiv. https://doi.org/10.1101/675280
Wang, W. Z., Oeschger, F. M., Lee, S., & Molnár, Z. (2009). High quality RNA from multiple brain regions simultaneously acquired by laser capture microdissection. BMC Molecular Biology, 10, 69.
Wang, W., Oeschger, F., Montiel, J., García-Moreno, F., Hoerder-Suabedissen, A., Krubitzer, L., … Molnár, Z. (2011). Comparative aspects of subplate zone studied with gene expression in sauropsids and mammals. Cerebral Cortex, 21(10), 2187-2203.
Wang, Q., Ng, L., Harris, J., Feng, D., Li, Y., Royall, J., … Zeng, H. (2017). Organization of the connections between claustrum and cortex in the mouse. Journal of Comparative Neurology, 525(6), 1317-1346.
Watakabe, A., Ohsawa, S., Ichinohe, N., Rockland, K. S., & Yamamori, T. (2014). Characterization of claustral neurons by comparative gene expression profiling and dye-injection analyses. Frontiers in Systems Neuroscience, 8, 98.
Watson, C., & Puelles, L. (2017). Developmental gene expression in the mouse clarifies the organization of the claustrum and related endopiriform nuclei. Journal of Comparative Neurology, 525(6), 1499-1508.
White, M. G., Cody, P. A., Bubser, M., Wang, H. D., Deutch, A. Y., & Mathur, B. N. (2017). Cortical hierarchy governs rat claustrocortical circuit organization. The Journal of Comparative Neurology, 525(6), 1347-1362.
White, M. G., & Mathur, B. N. (2018). The claustrum is required for reward acquisition under high cognitive demand. BioRxiv. https://doi.org/10.1101/390443
Willis, T. (1664). Cerebri Anatome: cui accessit nervorum descriptio et usus. London.
Zingg, B., Dong, H., Tao, H., & Zhang, L. (2018). Input-output organization of the mouse claustrum. Journal of Comparative Neurology, 526(15), 1-16.
Zolnik, T. A., Ledderose, J., Toumazou, M., Trimbuch, T., Oram, T., Rosenmund, C., … Larkum, M. E. (2020). Layer 6b is driven by intracortical long-range projection neurons. Cell Reports, 30, 3492-3505.