Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain
Abstract
The histochemical and morphological maturation of the mediodorsal nucleus (MD) and its connections were compared in human and rhesus monkey using acetylthiocholine iodide and Nissl methods. Histochemical analysis in fetuses, neonates, and adults of both primate species revealed that MD passes through three major stages of cholinesterase (ChE) reactivity. In Stage I (up to about 16 fetal weeks in man; 9 fetal weeks in monkey), ChE staining gradually increases in the MD nucleus and is intense in axons directed toward the frontal lobe through the internal and external capsules. In Stage II (about 16‐28 fetal weeks in man; about 9‐14 weeks in monkey), ChE staining in MD reaches peak intensity so that reaction product in the neurons and neuropil blackens the entire nucleus in both species. In favorable planes of section, ChE‐positive fibers appear to connect MD and the basal forebrain both of which stain intensely. ChE‐positive fibers can also be traced from the lateral margins of MD to the subplate zone beneath the developing frontal cortical plate where they continue to accumulate before later invading the cortex with heaviest concentration in presumptive layers 3 and 5. In Stage III (after 28 weeks of gestation to 6 postnatal months in man; from about 14 fetal weeks until 2 postnatal months in monkey), except for scattered positive cells, ChE staining gradually disappears in MD and the formerly dense laminar pattern in the cortex begins to lighten. The dramatic but transient increase in ChE staining in MD during fetal development as well as the sequentially related changes in its projections indicate that this early appearing enzyme may play a role in the development of the frontal lobe by influencing the differentiation of thalamoprefrontal connections.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A transient expression of the enzyme acetylcholinesterase seems to play a role in thalamocortical circuit formation.
“Alongside, a transient expression of the enzyme acetylcholinesterase seems to play a role in the thalamocortical circuit formation [218–220].”
From Development of prefrontal cortex (2022) · cites this paper as [218]
Cites
A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES
Karnovsky, M. J., & ROOTS, L. (1964) · Journal of Histochemistry & Cytochemistry · doi:10.1177/12.3.219 · Cited by 3,389 · see citing works
THE ASCENDING CHOLINERGIC RETICULAR SYSTEM: NEOCORTICAL, OLFACTORY AND SUBCORTICAL PROJECTIONS
Shute, C. C. D., & Lewis, P. R. (1967) · Brain · doi:10.1093/brain/90.3.497 · Cited by 1,120 · see citing works
The biology of cholinesterases
Silver, A. (1974) · Medical Entomology and Zoology · Cited by 890 · see citing works
The Molecular Forms of Cholinesterase and Acetylcholinesterase in Vertebrates
Massoulié, J., & Bon, S. (1982) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.05.030182.000421 · Cited by 818 · see citing works
THE WERNICKE-KORSAKOFF SYNDROME
Russell, R. W. R. (1972) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.35.2.277 · Cited by 815 · see citing works
Gebhart, G. F., & Schmidt, R. F. (2013) · Springer eBooks · doi:10.1007/978-3-642-28753-4_202463 · Cited by 806 · see citing works
Graybiel, A. M., & Ragsdale, C. W. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.11.5723 · Cited by 784 · see citing works
Prenatal genesis of connections subserving ocular dominance in the rhesus monkey
Rakic, P. (1976) · Nature · doi:10.1038/261467a0 · Cited by 677 · see citing works
Frontal Granular Cortex and Behavior.
Orbach, J. (1964) · Archives of General Psychiatry · doi:10.1001/archpsyc.1964.01720300109016 · Cited by 626 · see citing works
Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey
Kievit, J., & Kuypers, H. G. J. M. (1977) · Experimental Brain Research · doi:10.1007/bf00236173 · Cited by 497 · see citing works
Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex
Mesulam, M.-M., & Hoesen, G. W. V. (1976) · Brain Research · doi:10.1016/0006-8993(76)90385-1 · Cited by 426 · see citing works
Basal Forebrain and Hypothalamic Connection to Frontal and Parietal Cortex in the Rhesus Monkey
Kievit, J., & Kuypers, H. G. J. M. (1975) · Science · doi:10.1126/science.1114317 · Cited by 385 · see citing works
Goldman, P. S., & Galkin, T. W. (1978) · Brain Research · doi:10.1016/0006-8993(78)91103-4 · Cited by 315 · see citing works
THE STRUCTURE AND CONNECTIONS OF THE THALAMUS
Clark, W. E. L. G. (1932) · Brain · doi:10.1093/brain/55.3.406 · Cited by 284 · see citing works
Dorsal thalamic lesion in a noted case of human memory dysfunction
Squire, L. R., & Moore, R. Y. (1979) · Annals of Neurology · doi:10.1002/ana.410060607 · Cited by 283 · see citing works
Kostovic, I., & Rakic, P. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-01-00025.1984 · Cited by 270 · see citing works
Graybiel, A. M., & Berson, D. M. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90196-7 · Cited by 234 · see citing works
RAKIC, P. T. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901760103 · Cited by 219 · see citing works
Isseroff, A., Rosvold, H. E., Galkin, T. W., & Goldman, P. S. (1982) · Brain Research · doi:10.1016/0006-8993(82)90613-8 · Cited by 212 · see citing works
A histochemical study of cholinergic fibres in the cerebral cortex.
Krnjević, K., & Silver, A. (1965) · PubMed · Cited by 200 · see citing works
The ontogenetic development of the rabbit's diencephalon
Rose, J. E. (1942) · The Journal of Comparative Neurology · doi:10.1002/cne.900770105 · Cited by 160 · see citing works
Cholinesterases of the Central Nervous System with Special Reference to the Cerebellum
Silver, A. (1967) · International review of neurobiology · doi:10.1016/s0074-7742(08)60151-8 · Cited by 151 · see citing works
Butcher, L. L., & Hodge, G. K. (1976) · Brain Research · doi:10.1016/0006-8993(76)91022-2 · Cited by 149 · see citing works
Neurological Basis of Behavior
Grenell, R. G. (1959) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-195911000-00020 · Cited by 131 · see citing works
Pseudocholinesterase staining in the primary visual pathway of the macaque monkey
Graybiel, A. M., & Ragsdale, C. W. (1982) · Nature · doi:10.1038/299439a0 · Cited by 115 · see citing works
The early development of the human diencephalon
Gilbert, M. S. (1935) · The Journal of Comparative Neurology · doi:10.1002/cne.900620105 · Cited by 112 · see citing works
ACETYLCHOLINE SYSTEM AND NEURAL DEVELOPMENT
Filogamo, G., & Marchisio, P. C. (1971) · Elsevier eBooks · doi:10.1016/b978-0-12-512504-8.50008-1 · Cited by 108 · see citing works
Acetylcholinesterase in the developing forebrain.
Krnjević, K., & Silver, A. (1966) · PubMed · Cited by 105 · see citing works
Graybiel, A. M., & Ragsdale, C. W. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.2.1214 · Cited by 105 · see citing works
Cholinesterases: A Histochemical Contribution to the Solution of Some Functional Problems
Gerebtzoff, M. A. (2013) · Cited by 100 · see citing works
Metabolic Behaviour of Isozymes of Acetylcholinesterase
Davis, G. A., & Agranoff, B. W. (1968) · Nature · doi:10.1038/220277a0 · Cited by 92 · see citing works
Walker, A. E. (1940) · The Journal of Comparative Neurology · doi:10.1002/cne.900730107 · Cited by 89 · see citing works
ON THE CONNECTIONS OF THE MEDIAL CELL GROUPS OF THE THALAMUS
Clark, W. E. L. G., & BOGGON, R. H. (1933) · Brain · doi:10.1093/brain/56.1.83 · Cited by 83 · see citing works
Bilateral Symmetrical Degeneration of the Thalamus*†‡
Schulman, S. (1957) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-195710000-00002 · Cited by 79 · see citing works
Impaired Delayed Response From Thalamic Lesions
Schulman, S. (1964) · Archives of Neurology · doi:10.1001/archneur.1964.00460230027003 · Cited by 74 · see citing works
Dekaban, A. S. (1954) · The Journal of Comparative Neurology · doi:10.1002/cne.901000105 · Cited by 63 · see citing works
Parent, A., POIRIER, L. J., Boucher, R., & Butcher, L. L. (1977) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(77)90036-3 · Cited by 60 · see citing works
HISTOCHEMICAL EVIDENCE AND CONSEQUENCES OF THE OCCURRENCE OF ISOENZYMES OF ACETYLCHOLINESTERASE
KOELLE, W. A., HOSSAINI, K. S., AKBARZADEH, P., & Koelle, G. B. (1970) · Journal of Histochemistry & Cytochemistry · doi:10.1177/18.11.812 · Cited by 51 · see citing works
Ishii, T., & Friede, R. L. (1967) · International review of neurobiology · doi:10.1016/s0074-7742(08)60155-5 · Cited by 48 · see citing works
Multiple Nature of Acetylcholinesterase in Nerve Tissue
Bernsohn, J., Barron, K. D., & HESS, A. R. (1962) · Nature · doi:10.1038/195285a0 · Cited by 45 · see citing works
Ogren, M. P., & RAKIC, P. T. (1981) · Anatomy and Embryology · doi:10.1007/bf00318090 · Cited by 43 · see citing works
DEVELOPMENT OF ACETYLCHOLINESTERASE-ACTIVE STRUCTURES IN THE RAT ARCHICEREBELLAR CORTEX.
Csillik, B., Joó, F., Kása, P., Tomity, I., & KALMAN, G. (1964) · PubMed · Cited by 35 · see citing works
Wade, P. D., & Timiras, P. S. (2007) · Developmental Neuroscience · doi:10.1159/000112383 · Cited by 33 · see citing works
Genesis of Visual Connections in the Rhesus Monkey
RAKIC, P. T. (1979) · Springer eBooks · doi:10.1007/978-1-4684-3605-1_21 · Cited by 29 · see citing works
Koelle, G. B., Rickard, K. K., & Ruch, G. A. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.6012 · Cited by 29 · see citing works
Studies of the direct coloring thiocholine method for localizing cholinesterase activity
Broderson, S. H., Westrum, L. E., & Sutton, A. E. (1974) · Histochemistry and Cell Biology · doi:10.1007/bf00490269 · Cited by 17 · see citing works
The multiple forms of brain acetycholinesterase
H�ther, G., & Luppa, H. (1979) · Histochemistry and Cell Biology · doi:10.1007/bf00508016 · Cited by 13 · see citing works
Giacobini, G., & Filogamo, G. (1974) · Springer eBooks · doi:10.1007/978-3-642-65714-6_17 · Cited by 12 · see citing works
Vijayan, V. K., & Oschowka, J. A. (1977) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1977.tb10681.x · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pain and Its Effects in the Human Neonate and Fetus
Anand, K. J. S., & Hickey, P. R. (1987) · New England Journal of Medicine · doi:10.1056/nejm198711193172105 · Cited by 1,715 · see citing works
Normal development of brain circuits
Tau, G. Z., & Peterson, B. S. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.115 · Cited by 1,391 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
Kostović, I., & RAKIC, P. T. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902970309 · Cited by 912 · see citing works
Neurobiology of butyrylcholinesterase
Darvesh, S., Hopkins, D. A., & Geula, C. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1035 · Cited by 896 · see citing works
Do children really recover better? Neurobehavioural plasticity after early brain insult
Anderson, V. A., Spencer‐Smith, M. M., & WOOD, A. G. (2011) · Brain · doi:10.1093/brain/awr103 · Cited by 587 · see citing works
The development of cerebral connections during the first 20–45 weeks’ gestation
Kostović, I., & Milošević, N. J. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.07.001 · Cited by 568 · see citing works
Ontogeny of the human central nervous system: What is happening when?
de Graaf-Peters, V. B., & Hadders-Algra, M. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2005.10.013 · Cited by 559 · see citing works
The development of the subplate and thalamocortical connections in the human foetal brain
Kostović, I., & Judaš, M. (2010) · Acta Paediatrica · doi:10.1111/j.1651-2227.2010.01811.x · Cited by 462 · see citing works
Self-citationAkbarian, S. (1993) · Archives of General Psychiatry · doi:10.1001/archpsyc.1993.01820150016002 · Cited by 456 · see citing works
Uylings, H. B. M., & van Eden, C. G. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)62675-8 · Cited by 454 · see citing works
Lee, S. H., Ralston, H. J., Drey, E. A., Partridge, J. C., & Rosen, M. A. (2005) · JAMA · doi:10.1001/jama.294.8.947 · Cited by 413 · see citing works
Kostović, I. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.5.536 · Cited by 408 · see citing works
Akbarian, S. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830050061010 · Cited by 398 · see citing works
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
Anand, K. J. S., & Carr, D. B. (1989) · Pediatric Clinics of North America · doi:10.1016/s0031-3955(16)36722-0 · Cited by 382 · see citing works
Prenatal development of neurons in the human prefrontal cortex. II. A quantitative Golgi study
Mrzljak, L., Uylings, H. B. M., Kostović, I., & van Eden, C. G. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160408 · Cited by 316 · see citing works
Steriade, M., Paré, D., Parent, A., & Smith, Y. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90006-1 · Cited by 313 · see citing works
Petanjek, Z., Judas, M., Kostovic, I., & Uylings, H. B. M. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm124 · Cited by 273 · see citing works
Mechanisms of postnatal neurobiological development: Implications for human development
Webb, S. J., Monk, C. S., & Nelson, C. A. (2001) · Developmental Neuropsychology · doi:10.1207/s15326942dn1902_2 · Cited by 272 · see citing works
Neural histology and neurogenesis of the human fetal and infant brain
Kostović, I., Sedmak, G., & Judáš, M. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.12.043 · Cited by 259 · see citing works
Prenatal development of neurons in the human prefrontal cortex: I. A qualitative Golgi study
Mrzljak, L., Uylings, H. B. M., Kostović, I., & van Eden, C. G. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902710306 · Cited by 249 · see citing works
Novel Functions of Cholinesterases in Development, Physiology and Disease
Layer, P. G., & Willbold, E. (1994) · Progress in Histochemistry and Cytochemistry · doi:10.1016/s0079-6336(11)80046-x · Cited by 249 · see citing works
Chapter 9 Neuronal development in human prefrontal cortex in prenatal and postnatal stages
Mrzljak, L., Uylings, H. B. M., Van Eden, G. G., & Judáš, M. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62681-3 · Cited by 247 · see citing works
Development of Thalamocortical Connectivity during Infancy and Its Cognitive Correlations
Alcauter, S., Lin, W., Smith, J. K., Short, S. J., Goldman, B. D., Reznick, J. S., Gilmore, J. H., & Gao, W. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0796-14.2014 · Cited by 228 · see citing works
Pope, C., Chakraborti, T. K., Chapman, M., Farrar, J. D., & Arthun, D. (1991) · Toxicology · doi:10.1016/0300-483x(91)90061-5 · Cited by 242 · see citing works
Prenatal development of GABA‐ergic neurons in the neocortex of the rat
van Eden, C. G., Mrzljak, L., Voorn, P., & Uylings, H. B. M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890204 · Cited by 236 · see citing works
Bayatti, N., Moss, J. A., Sun, L. Y., Ambrose, P. M., Ward, J. F. H., Lindsay, S., & Clowry, G. J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm184 · Cited by 227 · see citing works
Kostović, I., & Judáš, M. (2002) · The Anatomical Record · doi:10.1002/ar.10069 · Cited by 215 · see citing works
Judáš, M., Radoš, M., Milošević, N. J., Hrabač, P., Štern-Padovan, R., & Kostović, I. (2005) · PubMed Central · Cited by 190 · see citing works
Development of the Human Cortex and the Concept of “Critical” or “Sensitive” Periods
Uylings, H. B. M. (2006) · Language Learning · doi:10.1111/j.1467-9922.2006.00355.x · Cited by 189 · see citing works
Small, D. H., Michaelson, S., & Sberna, G. (1996) · Neurochemistry International · doi:10.1016/0197-0186(95)00099-2 · Cited by 188 · see citing works
Kostović, I., Milošević, N. J., Radoš, M., Sedmak, G., Benjak, V., Srzentić, M. K., Vasung, L., Čuljat, M., Radoš, M., Hüppi, P. S., et al. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0496-0 · Cited by 176 · see citing works
Exploring early human brain development with structural and physiological neuroimaging
Vasung, L., Abaci Turk, E., Ferradal, S. L., Sutin, J., Stout, J. N., Ahtam, B., Lin, P.-Y., & Grant, P. E. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.07.041 · Cited by 177 · see citing works
Neurodevelopmental Changes of Fetal Pain
Lowery, C. L., Hardman, M., Manning, N., Clancy, B., Hall, R. W., & Anand, K. J. S. (2007) · Seminars in Perinatology · doi:10.1053/j.semperi.2007.07.004 · Cited by 160 · see citing works
Insights From In Vitro Fetal Magnetic Resonance Imaging of Cerebral Development
Kostović, I., & Vasung, L. (2009) · Seminars in Perinatology · doi:10.1053/j.semperi.2009.04.003 · Cited by 157 · see citing works
Vasung, L., Huang, H., Jovanov‐Milošević, N., Pletikos, M., Mori, S., & Kostović, I. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01260.x · Cited by 169 · see citing works
Kostović, I. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90077-1 · Cited by 153 · see citing works
Kostović, I., & Judáš, M. (2006) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162206000831 · Cited by 150 · see citing works
Zecevic, N., & Verney, C. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903510404 · Cited by 149 · see citing works
Robertson, R. T. (1987) · Neuroscience Letters · doi:10.1016/0304-3940(87)90531-3 · Cited by 147 · see citing works
A Century of Progress in Corticoneurogenesis: From Silver Impregnation to Genetic Engineering
RAKIC, P. T. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk036 · Cited by 142 · see citing works
Ontogenesis of goal-directed behavior: anatomo-functional considerations
Kostović, I., Judaš, M., Petanjek, Z., & Šimić, G. (1995) · International Journal of Psychophysiology · doi:10.1016/0167-8760(94)00081-o · Cited by 139 · see citing works
Cholinergic innervation of the human thalamus: Dual origin and differential nuclear distribution
Heckers, S., Geula, C., & Mesulam, M. M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903250107 · Cited by 132 · see citing works
Growth of Thalamocortical Fibers to the Somatosensory Cortex in the Human Fetal Brain
Krsnik, Ž., Majić, V., Vasung, L., Huang, H., & Kostović, I. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00233 · Cited by 127 · see citing works
Kostović, I. (1991) · Progress in Brain Research · doi:10.1016/s0079-6123(08)62682-5 · Cited by 127 · see citing works
Kostović, I., Judáš, M., & Sedmak, G. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.09.005 · Cited by 121 · see citing works
Vasung, L., Lepage, C., Radoš, M., Pletikos, M., Goldman, J. S., Richiardi, J., Raguž, M., Fischi-Gómez, E., Karama, S., Hüppi, P. S., et al. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00011 · Cited by 121 · see citing works
Verney, C., Lebrand, C., & Gaspar, P. (2002) · The Anatomical Record · doi:10.1002/ar.10089 · Cited by 119 · see citing works
Kostović, I., & JUDAS, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.018 · Cited by 119 · see citing works
Sims, K. S., & Williams, R. S. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90440-f · Cited by 118 · see citing works
Duque, A., Krsnik, Ž., Kostović, I., & RAKIC, P. T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610078113 · Cited by 118 · see citing works
Khan, S., Vasung, L., Marami, B., Rollins, C. K., Afacan, O., Ortinau, C. M., Yang, E., Warfield, S. K., & Gholipour, A. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2018.08.030 · Cited by 115 · see citing works
Gangliosides in the human brain development and aging
Kraĉun, I., Rösner, H., Drnovsek, V., Vukelić, Ž., Ćosović, Č., Trbojević-Čepe, M., & Kubat, M. (1992) · Neurochemistry International · doi:10.1016/0197-0186(92)90057-x · Cited by 113 · see citing works
Höhmann, C. F., & Ebner, F. F. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90045-8 · Cited by 112 · see citing works
Mooney‐Leber, S. M., & Brummelte, S. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.001 · Cited by 114 · see citing works
Spontaneous Electrical Activity in the Human Fetal CortexIn Vitro
Moore, A. R., Zhou, W., Jakovčevski, I., Zečević, N., & Antic, S. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3886-10.2011 · Cited by 109 · see citing works
The development of the nociceptive brain
Verriotis, M., Chang, P., Fitzgerald, M., & Lorenzo Fabrizi, D. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.07.026 · Cited by 98 · see citing works
Subplate in the developing cortex of mouse and human
Wang, W. Z., Hoerder‐Suabedissen, A., Oeschger, F. M., Bayatti, N., Ip, B. K., Lindsay, S., Supramaniam, V. G., Srinivasan, L., Rutherford, M., Møllgård, K., et al. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01274.x · Cited by 100 · see citing works
Kostović, I. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101883 · Cited by 102 · see citing works
Cholinesterases in neural development: new findings and toxicologic implications.
Brimijoin, S., & Koenigsberger, C. (1999) · Environmental Health Perspectives · doi:10.1289/ehp.99107s159 · Cited by 99 · see citing works
Schwarz, M., Glick, D., Loewenstein, Y., & Soreq, H. (1995) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(95)00019-d · Cited by 97 · see citing works
Meyer, G., & González‐Hernández, T. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903380302 · Cited by 96 · see citing works
Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study
Travis, K., Ford, K., & Jacobs, B. (2005) · Developmental Neuroscience · doi:10.1159/000086707 · Cited by 89 · see citing works
Kostović, I., Radoš, M., Srzentić, M. K., & Krsnik, Ž. (2021) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlab024 · Cited by 90 · see citing works
The antenatal development of fetal behavioral patterns assessed by four-dimensional sonography
Kurjak, A., Carrera, J. M., Medic, M. G., Azumendi, G., Andonotopo, W., & Stanojević, M. (2005) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767050400029657 · Cited by 89 · see citing works
Gaining insight of fetal brain development with diffusion MRI and histology
Huang, H., & Vasung, L. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.06.005 · Cited by 88 · see citing works
The significance of the subplate for evolution and developmental plasticity of the human brain
Judáš, M., Sedmak, G., & Kostović, I. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00423 · Cited by 86 · see citing works
Huntley, G. W., & Jones, E. G. (1990) · Journal of Neurocytology · doi:10.1007/bf01217298 · Cited by 84 · see citing works
Morphogenic role for acetylcholinesterase in axonal outgrowth during neural development.
Bigbee, J. W., Sharma, K. V., Gupta, J. J., & Dupree, J. L. (1999) · Environmental Health Perspectives · doi:10.1289/ehp.99107s181 · Cited by 81 · see citing works
Robertson, R. T., Mostamand, F., Kageyama, G. H., Gallardo, K. A., & Yu, J. Z. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90240-j · Cited by 80 · see citing works
Populations of subplate and interstitial neurons in fetal and adult human telencephalon
Judáš, M., Sedmak, G., Pletikos, M., & Milošević, N. J. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01284.x · Cited by 79 · see citing works
Robertson, R. T., Hanes, M. A., & Yu, J. Z. (1988) · Developmental Brain Research · doi:10.1016/0165-3806(88)90165-4 · Cited by 78 · see citing works
Issues of Assessment of Pain and Discomfort in Neonates
Stevens, B., Johnston, C. C., & GRUNAU, R. E. (1995) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1111/j.1552-6909.1995.tb02570.x · Cited by 77 · see citing works
Verney, C., Milosevic, A., Alvarez, C., & Berger, B. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903360303 · Cited by 77 · see citing works
Huntley, G. W., Benson, D. L., Jones, E. G., & Isackson, P. J. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90103-4 · Cited by 75 · see citing works
3D global and regional patterns of human fetal subplate growth determined in utero
Corbett-Detig, J., Habas, P. A., Scott, J. A., Kim, K., Rajagopalan, V., McQuillen, P. S., Barkovich, A. J., Glenn, O. A., & Studholme, C. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0286-5 · Cited by 72 · see citing works
Letinić, K., & Kostović, I. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970804)384:3 · Cited by 3 · see citing works
Sweeney, J. E., Höhmann, C. F., Oster‐Granite, M. L., & Coyle, J. T. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90384-9 · Cited by 73 · see citing works
Postnatal changes in the distribution of acetylcholinesterase in kitten striate cortex
Bear, M. F., Carnes, K. M., & Ebner, F. F. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902370408 · Cited by 72 · see citing works
Vasung, L., Raguž, M., Kostović, I., & Takahashi, E. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00348 · Cited by 69 · see citing works
Robertson, R. T., Tijerina, A. A., & Gallivan, M. E. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90209-3 · Cited by 71 · see citing works
The multiple biological roles of the cholinesterases
Silman, I. (2020) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2020.12.001 · Cited by 69 · see citing works
Kostović, I., Išasegi, I. Ž., & Krsnik, Ž. (2018) · Journal of Anatomy · doi:10.1111/joa.12920 · Cited by 67 · see citing works
Judáš, M., Sedmak, G., & Pletikos, M. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01283.x · Cited by 65 · see citing works
Kostović, I., Srzentić, M. K., Benjak, V., Milošević, N. J., & RadoÅ¡, M. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00139 · Cited by 66 · see citing works
Huntley, G. W., & Jones, E. G. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90055-s · Cited by 65 · see citing works
Xu, Y., Cao, M., Liao, X., Xia, M., Wang, X., Jeon, T., Ouyang, M., Chalak, L. F., Rollins, N. K., Huang, H., et al. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy302 · Cited by 59 · see citing works
What are the Best Animal Models for Testing Early Intervention in Cerebral Palsy?
Clowry, G. J., Basuodan, R., & Chan, F. (2014) · Frontiers in Neurology · doi:10.3389/fneur.2014.00258 · Cited by 62 · see citing works
Verney, C. (1999) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19990701)46:1 · Cited by 62 · see citing works
New data about embryonic and fetal neurodevelopment and behavior obtained by 3D and 4D sonography
Salihagič-Kadić, A., Kurjak, A., Medic, M. G., Andonotopo, W., & Azumendi, G. (2005) · Journal of Perinatal Medicine · doi:10.1515/jpm.2005.086 · Cited by 60 · see citing works
Kostović, I., Škavić, J., & Strinović, D. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90795-1 · Cited by 58 · see citing works
Self-citationEarly vocal contact and music in the NICU: new insights into preventive interventions
Filippa, M., Lordier, L., de Almeida, J. S., Monaci, M. G., Adam‐Darqué, A., Grandjean, D., Kuhn, P., & Hüppi, P. S. (2019) · Pediatric Research · doi:10.1038/s41390-019-0490-9 · Cited by 57 · see citing works
Fetal pain perception and pain management
de Velde, M. V., Jani, J. C., Buck, F. D., & Deprest, J. A. (2006) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2006.02.012 · Cited by 58 · see citing works
Vasung, L., Milošević, N. J., Pletikos, M., Mori, S., Judáš, M., & Kostović, I. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0279-4 · Cited by 56 · see citing works
Early areal differentiation of the human cerebral cortex: Entorhinal area
Kostović, I., Petanjek, Z., & Judáš, M. (1993) · Hippocampus · doi:10.1002/hipo.450030406 · Cited by 56 · see citing works
Berger, B., Alvarez, C., & Goldman‐Rakic, P. S. (1993) · Hippocampus · doi:10.1002/hipo.450030305 · Cited by 56 · see citing works
Self-citationNeuronal plasticity induced by neonatal monocular (and binocular) enucleation
Toldi, J. (1996) · Progress in Neurobiology · doi:10.1016/0301-0082(95)00038-0 · Cited by 55 · see citing works
Popken, G. J., & Farel, P. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970915)386:1 · Cited by 117 · see citing works
Kostović, I., Sedmak, G., Vukšić, M., & Judáš, M. (2014) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12333 · Cited by 54 · see citing works
- Authors
- Kostovic, I., & Goldman‐Rakic, P. S.
- Affiliations
- Yale University (US)
- Corresponding author
- Goldman‐Rakic, Patricia S.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1983-10
- Volume
- 219
- Issue
- 4
- Pages
- 431-447
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2012514021
- Cited by
- 260
- References
- 49
- Citations by year
- 2025: 2 · 2024: 7 · 2023: 5 · 2022: 6 · 2021: 5 · 2020: 10 · 2019: 5 · 2018: 12 · 2017: 6 · 2016: 6 · 2015: 3 · 2014: 10 · 2013: 7 · 2012: 7
- FWCI
- 3.64
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology › Cholinesterase and Neurodegenerative Diseases
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- mediodorsal nucleus, thalamus, cholinesterase, acetylthiocholine iodide, frontal lobe development, fetal brain development, rhesus monkeys, human brain, subplate, developmental maturation
- MeSH terms
- Animals, Cholinesterases, Histocytochemistry, Humans, Macaca, Macaca mulatta, Neural Pathways, Staining and Labeling, Thalamic Nuclei, Tissue Distribution
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
