2007;104:76527. Age-dependent effects of lesioning the mesocortical dopamine system upon prefrontal cortex morphometry and PFC-related behaviors. Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Nature. You are using a browser version with limited support for CSS. Nosarti C, Nam KW, Walshe M, Murray RM, Cuddy M, Rifkin L, et al. Science. 2013;49:226471. A novel cytoarchitectonic area induced experimentally within the primate visual cortex. Kabanova A, Pabst M, Lorkowski M, Braganza O, Boehlen A, Nikbakht N, et al. 1986;320:1726. bioRxiv. Diffusion tensor imaging provides evidence of possible axonal overconnectivity in frontal lobes in autism spectrum disorder toddlers. Sprinfield, IL: Thomas; 1982. Cell Tissue Res. 2016;221:53561. 2018;28:41120. Maternal metabolic disorders including diabetes and obesity can pose another threat to the unborn child as placental dysfunctioning alters the prenatal exposure to nutrients and toxins [312,313,314]. 1979;156:11552. 2015;2:2. The part of the brain behind the forehead, called the prefrontal cortex, is one of the last parts to mature. 2011;294:161523. The period of synapticdecline in human PFC, which starts during childhood, is initially dramatic and continues during adolescence and extends at a slower, but statistically significant rate into the 3rd decade of life (Fig. 2015;39:85362. 1990;28:51727. J Neurodev Disord. J Neurochem. The prefrontal cortex (PFC) relates to the portion of the brain located on the anteriormost portion of the frontal lobe, occupying portions of all three surfaces of the frontal lobe (orbital, medial and lateral surfaces). Arnsten AF. 2018;360:815. Mesocortical dopamine neurons operate in distinct temporal domains using multimodal signaling. Neurogenic radial glia in the outer subventricular zone of human neocortex. 1998;94:32537. J Neurosci. Laje G, Morse R, Richter W, Ball J, Pao M, Smith AC. Another field of recent study is the perinatal exposure to pharmaceuticals given to treat the pregnant mother. 2004;46:4653. J Neurosci. Carr DB, Sesack SR. Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals. Neuronal network dysfunction in a model for Kleefstra syndrome mediated by enhanced NMDAR signaling. Am J Med Genet Part C Semin Med Genet. Disruptions in PFC network activity often further aggravates the already compromised neurocognitive development in these children [365, 366]. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. Decreased dendritic branching in frontal, motor and limbic cortex in Rett syndrome compared with trisomy 21. Molnar Z, Hoerder-Suabedissen A. Allin M, Henderson M, Suckling J, Nosarti C, Rushe T, Fearon P, et al. Hernan AE, Alexander A, Jenks KR, Barry J, Lenck-Santini PP, Isaeva E, et al. Mol Neurobiol. Kolk, S.M., Rakic, P. Development of prefrontal cortex. Booij L, Tremblay RE, Szyf M, Benkelfat C. Genetic and early environmental influences on the serotonin system: consequences for brain development and risk for psychopathology. Science 2017;358:47882. The origin of species-specific distinctions can be traced either to the new or phylogenetically conserved genes that act at the time of the neural stem cells exit from the mitotic cycle and generate a different outcome, depending on the evolutionary context by interacting with a postmitotic neuron. More holistic studies into the extrasynaptic neurotrophic functions of neurotransmitters during prefrontal development might also provide more understanding of their potential roles in the etiology of NDDs and eventually will enable us to design critical developmental windows in which we may be able to intervene. The prefrontal cortex (PFC) receives input from all other cortical regions and functions to plan and direct motor, cognitive, affective, and social behavior across time. BMJ Open. 2019. Focal epileptiform activity in the prefrontal cortex is associated with long-term attention and sociability deficits. Curr Psychiatry Rep. 2009;11:3938. Lauder JM, Bloom FE. 2008;172:4571. Quantitative assessment of prefrontal cortex in humans relative to nonhuman primates. In addition, DRN serotonergic neurons are controlled by glutamatergic projections from the PFC [152, 207,208,209]. It is also called the 'frontal granular cortex' and 'frontal association cortex'. This brain region has been implicated in planning complex cognitive behavior, personality expression, decision making, and moderating social behaviour. These children often have various conditions that are collectively known as Fetal Alcohol Spectrum Disorder (FASD), which includes FAS and a condition known as Alcohol-related Neurodevelopmental Disorder (ARND). The Feinberg hypothesis revisited. Silver DL, Rakic P, Grove EA, Haydar TF, Hensch TK, Huttner WB, et al. Development of prefrontal cortex During evolution, the cerebral cortex advances by increasing in surface and the introduction of new cytoarchitectonic areas among which the prefrontal cortex (PFC) is considered to be the substrate of highest cognitive functions. Cereb Cortex. When neurites to and from the PFC reach their final target position, an immature synapse is generated under the influence of, among others, cell adhesion molecules and reelin [88, 89]. Cell. 5, No. Early Hum Dev. 2019;116:708994. Bailey CD, Alves NC, Nashmi R, De Biasi M, Lambe EK. 2019;20:16176. The basic activity of this brain region is considered to be orchestration of thoughts and actions . Perturbed developmental serotonin signaling affects prefrontal catecholaminergic innervation and cortical integrity. Developmental Cogn Neurosci. J Neurosci. Science 1983;219:14414. The period of teenage till young adulthood is critical as in this time frame; the prefrontal cortex is still developing. 2013;81:74551. 2008;99:152334. Pharmacol Rev. Mi D, Li Z, Lim L, Li M, Moissidis M, Yang Y, et al. Dopamine, cocaine and the development of cerebral cortical cytoarchitecture: a review of current concepts. Shaw P, Rabin C. New insights into attention-deficit/hyperactivity disorder using structural neuroimaging. Our experiences, social interactions, and learning can impact the development of this region. NeuroImage Clin. Teng T, Gaillard A, Muzerelle A, Gaspar P. EphrinA5 signaling is required for the distinctive targeting of raphe serotonin neurons in the forebrain. Oberst P, Fievre S, Baumann N, Concetti C, Bartolini G, Jabaudon D. Temporal plasticity of apical progenitors in the developing mouse neocortex. J Neurosci. A similar surge in regional-specific dopaminergic connectivity to the PFC can be observed in primates, including human modulating local microcircuits [165,166,167,168,169]. Schratt G. microRNAs at the synapse. Felten DL, Hallman H, Jonsson G. Evidence for a neurotropic role of noradrenaline neurons in the postnatal development of rat cerebral cortex. 1988;269:5872. Pharmacological treatment of disruptive behavior in Smith-Magenis syndrome. Although still debated, the human frontal lobe seems to have evolved three times larger than that of our closest living relatives, the great apes. Article Kiryushko D, Berezin V, Bock E. Regulators of neurite outgrowth: role of cell adhesion molecules. NeuroImage. Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. In fact, neurotransmitter receptors are found to be expressed by progenitor cells throughout development [231]. It is now generally accepted that the etiology of many NDDs is considered to be multifactorial. Premature aging phenotype in mice lacking high-affinity nicotinic receptors: region-specific changes in layer V pyramidal cell morphology. More on the role of the PFC in cognitive control and executive functioning can be found in this volume in the reviews by Robbins and Friedman (I.6) and Menon and DEsposito (I.7). Bang SJ, Jensen P, Dymecki SM, Commons KG. Activation of the medial prefrontal cortex reverses cognitive and respiratory symptoms in a mouse model of rett syndrome. A subset of the medial part of the ventral tegmental area (VTA) starts to project to prefrontal subdomains around E15/E16 (rodent) and week 1013 in human [155,156,157,158]. More on evolution of the prefrontal cortex can be found in this volume, part I, chapter 1. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW. 2015;18:87282. Child Neuropsychol. Arid1b haploinsufficient mice reveal neuropsychiatric phenotypes and reversible causes of growth impairment. The PFC, as the seat of our higher-order cognitive functions, continues to develop into adulthood [52, 243]. Rivell A, Mattson MP. Proc Natl Acad Sci USA. New research is helping scientists learn about areas that are crucial to emotional development, and how our surroundings fit into the picture. Front Cell Neurosci. Development of cholinergic innervation in the hippocampal formation of the rat. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. In fact, it has been argued that the human brain possesses prefrontal regions that are both qualitatively and functionally exclusive [15]. J Neurocytol. These days, selective elimination or stabilization is commonly called pruning, and this refinement of the differentiating cortical network via pruning of dendritic branches, and/or efferent/afferent projections, is an important process to fine-tune the meticulous intricate prefrontal network [100, 101]. The changing number of cells in the human fetal forebrain and its subdivisions: a stereological analysis. Internet Explorer). Chronic stress increases prefrontal inhibition: a mechanism for stress-induced prefrontal dysfunction. 2001;240:14356. Therefore, the early childhood PFC contains a 23 fold higher density of dendritic spines compared to the adult PFC. Nat Rev Neurosci. A multitude of cortical and subcortical targets are progressively innervated by developing glutamatergic projections from the PFC itself such as the various thalamic regions. 2018;12:67. Fertuzinhos S, Krsnik Z, Kawasawa YI, Rasin MR, Kwan KY, Chen JG, et al. J Neuroimmunol. 2008;172:36. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. 2019;2:234. As the prefrontal cortex develops, so does one's capacity for uniqueness-- the recognition and also understanding that everyone possesses special . In many neurodevelopmental disorders (NDDs) the developing dopamine system is affected playing a role in the diverse symptoms of these disorders [179]. In: Plum F, editor. Eur J Neurosci. Gray matter continues to increase well into adolescence [52]. Komitova M, Xenos D, Salmaso N, Tran KM, Brand T, Schwartz ML, et al. The most ventral subdomain of the mPFC is the infralimbic cortex (IL) and is involved in coping with chronic stress eventually leading to structural changes and prefrontal dysfunction [5,6,7,8,9,10,11]. 2019; https://www.biorxiv.org/content/10.1101/2019.12.31.891036v1. Borrell V, Reillo I. Vitalis T, Parnavelas JG. Work of Cholfin and Rubenstein in mice provide experimental evidence that the PFC can expand differentially and independently of the growth rate of the other areas [30, 31] and that its size can be regulated at early stages by the change of expression of specific growth factors before they receive the afferent axonal input [32]. Thank you for visiting nature.com. Kubrusly RC, Bhide PG. A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex. Huang C, Liu T, Wang Q, Hou W, Zhou C, Song Z, et al. Hilgetag CC, Barbas H. Are there ten times more glia than neurons in the brain? Proc Natl Acad Sci USA. Once the serotonergic projections have arrived within cortical areas, they are able to make contacts with Cajal Retzius cells within the MZ, thereby raising the possibility of playing a role in neuronal migration [122,123,124]. 2018;12:70. Wise SP. Forward frontal fields: phylogeny and fundamental function. Genesis of neurons destined for the PFC is completed by E90, before completion of neurogenesis in the primary visual cortex at E90 (Fig. Lim L, Pakan JMP, Selten MM, Marques-Smith A, Llorca A, Bae SE, et al. 2016;26:64554. Heterogeneous organization of the locus coeruleus projections to prefrontal and motor cortices. 2000;119:3345. Elevated prefrontal oscillations and hippocampal-prefrontal theta coherence could be observed after FLE [388]. Narboux-Neme N, Pavone LM, Avallone L, Zhuang X, Gaspar P. Serotonin transporter transgenic (SERTcre) mouse line reveals developmental targets of serotonin specific reuptake inhibitors (SSRIs). Prefrontal cortex dysfunction in fragile X mice depends on the continued absence of fragile X mental retardation protein in the adult brain. J Comp Neurol. Celen C, Chuang JC, Luo X, Nijem N, Walker AK, Chen F, et al. Eur J Neurosci. Kates WR, Burnette CP, Bessette BA, Folley BS, Strunge L, Jabs EW, et al. The primary somatosensory cortex, as well as the primary motor cortex, mature earlier, however the dendritic trees and the density of spines within the subdomains of the PFC seem to be more complex [246,247,248,249]. 2002;448:186202. Functional and evolutionary insights into human brain development through global transcriptome analysis. Jay V, Chan FW, Becker LE. Similar structural and behavioral defects of the PFC can be observed in kids with prenatal exposure to opioids, cocaine, amphetamines and other drugs-of-abuse [322,323,324,325,326,327,328,329,330]. Naneix F, Marchand AR, Di Scala G, Pape JR, Coutureau E. Parallel maturation of goal-directed behavior and dopaminergic systems during adolescence. Neurobiol Dis. 2016;22:135867. NeuroImage. Cereb Cortex. 1999;38:25969. Trekking across the brain: the journey of neuronal migration. Variable environmental exposure to risk factors combined with variable genetic background makes it hard to pinpoint possible causes. Ayala R, Shu T, Tsai LH. New insights into the development of the human cerebral cortex. 2008;18:91529. Many food-derived molecules can reach the unborn baby in one form or another, and therefore could directly or indirectly influence brain development when crossing the immature blood-brain barrier and potentially affect PFC development [308]. Brain Res. 2003;53:10711. A Schematic representation of the site of the block dissection from the depth of the Sulcus Principalis (SP). Magnitude and heterogeneity of brain structural abnormalities in 22q11.2 deletion syndrome: a meta-analysis. Rotaru DC, van Woerden GM, Wallaard I, Elgersma Y. Alcohol Clin Exp Res. 2020;117:1003544. Neurochemistry Int. Turning of nerve growth cones induced by neurotransmitters. 47, 4157 (2022). Benes FM, Taylor JB, Cunningham MC. The intricate timely integration of all these neurotransmitter systems is essential for prefrontal functioning. Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Dev Neurosci. 2012;13:18. 1991;40:36374. [396]. 2006;9:1739. Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. 2019;42:70926. Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S, et al. Neuropharmacology. Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. 2020;135:104706. Adv Exp Med Biol. Rakic P. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Cell Cycle. Nature. 1999;285:9069. Eventually, the mature mesoprefrontal system is involved in attention, behavioral flexibility, action planning, sustainability of motivational and affective states, working memory and memory consolidation which is mediated in parallel by catecholaminergic pathways [169, 174,175,176,177,178]. It is at the front of the frontal lobe, which is immediately behind the forehead. Noradrenergic alpha1-adrenoceptor actions in the primate dorsolateral prefrontal cortex. Adolescent Maturity and the Brain: The Promise and Pitfalls of 2019;41:6778. Prospective associations between dietary patterns and cognitive performance during adolescence. 2012;232:23344. 2003;13:11522. Kovacs-Balint ZA, Payne C, Steele J, Li L, Styner M, Bachevalier J, et al. 2020;36:5679. Holmes GL. The PMH is atpresent universally accepted even by its initial opponents (e.g., [29]). Defects in embryonic neurogenesis and initial synapse formation in the forebrain of the Ts65Dn mouse model of Down syndrome. Manitt C, Mimee A, Eng C, Pokinko M, Stroh T, Cooper HM, et al. Control processes mediated by the PFC are hampered. Raper J, Kovacs-Balint Z, Mavigner M, Gumber S, Burke MW, Habib J, et al. Fetal Brain Development: When Your Baby Develops a Brain - What to Expect Neuroendocrinology. Prefrontal Cortex: Anatomy, Function, and Conditions - Verywell Health Gestational factors throughout fetal neurodevelopment: the serotonin link. Tang S, Xu S, Waddell J, Zhu W, Gullapalli RP, Mooney SM. 2010;2:99108. Similarly, we can find lead and other pollutants to be damaging to the developing brain and PFC [331,332,333,334]. Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. 1 In particular, magnetic resonance imaging (MRI) studies have discovered that myel. Howell CJ, Sceniak MP, Lang M, Krakowiecki W, Abouelsoud FE, Lad SU, et al. Cholfin JA, Rubenstein JL. Cell. Chailangkarn T, Trujillo CA, Freitas BC, Hrvoj-Mihic B, Herai RH, Yu DX, et al. Although the basic principles of cortical development may be similar in all mammals, the modifications of developmental events during millennia of primate evolution produce not only quantitative but also qualitative changes of its cellular structure and synaptic circuitry [13, 20]. J Comp Neurol. Elston GN, Benavides-Piccione R, Elston A, Manger PR, Defelipe J. Pyramidal cells in prefrontal cortex of primates: marked differences in neuronal structure among species. 2017;16:126670. Cognitive abilities are affected due to a developmental delay including the maturation of brain areas such as the PFC [293]. Skorput AG, Gupta VP, Yeh PW, Yeh HH. 1995;7:124. 2013;1:45. Lefevre J, Germanaud D, Dubois J, Rousseau F, de Macedo Santos I, Angleys H, et al. Likewise, the axons of the corpus callosum, as well as other large axonal tracts in the macaque cortex, including PFC, are grossly overproduced before decreasing to the adult level [95,96,97]. Proc Natl Acad Sci USA. Neuroscientist. Neurosci Biobehav Rev. 1974;36:13041. 2016;40:12534. 2005;210:4117. 2001;305:17786. This is also the case for the inhibitory network where the interneurons mature extensively with a sharp increase in the dendritic spine formation but also in terms of their intrinsic as well as their network properties as was shown in mice [85, 86]. The prolonged maturation of the PFC depends largely on the coordinated action of various external factors. Postnatal alterations in dopaminergic markers in the human prefrontal cortex. 2012;18:14137. NeuroImage. Bortel A, Nowak P, Brus R. Neonatal DSP-4 treatment modifies GABAergic neurotransmission in the prefrontal cortex of adult rats. Kas A, Soret M, Pyatigoskaya N, Habert MO, Hesters A, Le Guennec L, et al. Epilepsy Res. Llinares-Benadero C, Borrell V. Deconstructing cortical folding: genetic, cellular and mechanical determinants. Gao M, Liu CL, Yang S, Jin GZ, Bunney BS, Shi WX. Garcia LP, Van de Wijer L, Hanswijk SI, Rando J, Witteveen JS, Middelman A, et al. 2019;235:43251. 2013;7:143. Nature. Nature. Sidman RLRP. J Chem Neuroanat. 2016;70:412. Anat Rec. Multiple fetuses per pregnancy, intrauterine growth restriction (IUGR, due to placental failure other than by causes described above), X-ray, UV, nuclear or cosmic radiation, (ultra)sound as well as high temperature, preterm birth or hypoxia whether or not by traumatic causes can pose serious threats to proper corticogenesis as well [349,350,351,352,353,354,355,356]. A new and interesting finding is that there appears to be a major change in the levels of various metabolites in the PFC of autistic individuals [379]. Neyens LG, Aldenkamp AP, Meinardi HM. But even before the cholinergic projections arrive in the cortical areas, the nicotinic and muscarinic receptors are expressed on neural progenitors playing a role in proliferation/differentiation and axonal guidance events [214,215,216,217]. C Illustration of the dynamics of major developmental events and diversity of progenitors involved in the development of primate cerebral neocortex based on studies of Rakic, with permission from Silver et al. Brain Struct Funct. 2007;212:14979. Cereb Cortex. It has been speculated that, as the PFC takes so long to fully mature, it also has the largest critical window of all developing brain areas. Morin EL, Howell BR, Feczko E, Earl E, Pincus M, Reding K, et al. Reynolds LM, Pokinko M, Torres-Berrio A, Cuesta S, Lambert LC, Del Cid Pellitero E. et al. The Locus Coeruleus (LC) in the brainstem sends out its noradrenergic axonal projections to the PFC as early as E16/17 (rodent) and week 1013 in human [130,131,132]. Muffat J, Li Y, Yuan B, Mitalipova M, Omer A, Corcoran S, et al. Petanjek Z, Judas M, Simic G, Rasin MR, Uylings HB, Rakic P, et al. Neurotox Res. Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Sci Rep. 2016;6:26865. Altered synaptic ultrastructure in the prefrontal cortex of Shank3-deficient rats. 2016;113:542934. Prog brain Res. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J. Thompson SM, Kallarackal AJ, Kvarta MD, Van Dyke AM, LeGates TA, Cai X. Like serotonin, noradrenergic axons make contact with the Cajal Retzius cells in the marginal zone, suggesting a role in the laminar formation of cortical regions [132, 142, 143]. Cell Rep. 2014;9:213951. White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Luciana and Nelson's study showed that in normal children, aged 4-8 years, the prefrontal working memory system emerges at around the age of 4 and improves between 5 and 7 years of age [ 94 ], and capacity of visual short-term memory increases also substantially between 5 and 11 years of age [ 95 ]. 2010;30:14595609. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL. Toxoplasmosis, Other (syphilis, varicella-zoster, parvovirus B19), Rubella, Cytomegalovirus (CMV), and Herpes infections. Intrauterine growth restriction increases impulsive behavior and is associated with altered dopamine transmission in both medial prefrontal and orbitofrontal cortex in female rats. It has furthermore been shown that dopamine and GABA interactions can influence these processes [187, 188]. Cereb Cortex. Neuropsychologia. In nonhuman primates this is characterized by risk-taking, novelty seeking, and increased vigilance; whereas in rodents by play behavior, increased exploratory activity and impulsivity are peaking [245]. All this is especially important in light of (anti-depressant) use of pharmacological drugs during pregnancy as they can interfere with these early signaling pathways and hamper the structural development of brain areas including the PFC. Proc Natl Acad Sci USA. Money KM, Stanwood GD. Neuron number and size in prefrontal cortex of children with autism. 1990;85:25782. Proc Natl Acad Sci USA. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Epigenetic regulatory factors such as microRNAs (miRNAs) play an important role in this process by modulating dendritic and synaptic maturation [90, 91]. The noradrenergic system influences the fate of Cajal-Retzius cells in the developing cerebral cortex. Kable JA, Coles CD, Mattson SN. To better understand why that is, Shibata and Pattabiraman for the second study focused on the gene CBLN2, which is enriched in the prefrontal cortex and plays a key role in forming these connections. 2008;13:24752. 2010;107:1156772. Recurrent de novo mutations in neurodevelopmental disorders: properties and clinical implications. A transient placental source of serotonin for the fetal forebrain. Prader-Willi syndrome (PWS) is a disorder in which imprinted genes on chromosome 15 are affected andis characterized by increased volume of prefrontal subdomains important in the reward circuitry [300, 301]. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. PubMed Grewen K, Burchinal M, Vachet C, Gouttard S, Gilmore JH, Lin W, et al. Mol Psychiatry. Cell Mol life Sci. 2003;25:24556. 2021;226:196172. 2009;2:8. 1995;18:41824. Miyata T, Kawaguchi A, Okano H, Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Reversal of social recognition deficit in adult mice with MECP2 duplication via normalization of MeCP2 in the medial prefrontal cortex. Science. Proulx E, Young EJ, Osborne LR, Lambe EK. 2005;25:501323. Darcq E, Warnault V, Phamluong K, Besserer GM, Liu F, Ron D. MicroRNA-30a-5p in the prefrontal cortex controls the transition from moderate to excessive alcohol consumption. PubMed Central Early features of corticogenesis can be recapitulated reliably; however the later stages in development still need to be optimized. 2017;27:462434. Hansen DV, Lui JH, Parker PR, Kriegstein AR. The effect of neonatal 6-hydroxydopamine treatment on synaptogenesis in the visual cortex of the rat. The neurocognitive phenotype in velo-cardio-facial syndrome: a developmental perspective. Kurochkin I, Khrameeva E, Tkachev A, Stepanova V, Vanyushkina A, Stekolshchikova E, et al. Garcia-Cabezas MA, Barbas H, Zikopoulos B. Ge WP, Miyawaki A, Gage FH, Jan YN, Jan LY. Traditionally, pregnant women were warned for TORCH (TOxoplasmosis, Rubella, Cytomegalovirus, and Herpes simplex viruses type 1 and 2) infections especially during the first two trimesters of pregnancy as they were shown to cause severe congenital abnormalities [337]. 2000;10:22042. Prog Brain Res. Kosik KS, Nowakowski T. Evolution of new miRNAs and cerebro-cortical development. 2021;226:117574. Strngmann Forum Reports, vol. Biol Psychiatry. 1990;8:21721. 2020;10:41. Nygaard E, Slinning K, Moe V, Due-Tonnessen P, Fjell A, Walhovd KB. Understanding the Teen Brain - Health Encyclopedia - University of 2018;68:1326. Proc Natl Acad Sci USA. Nousen EK, Franco JG, Sullivan EL. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, et al. Barbas H, Garcia-Cabezas MA. 2020;11:2534. Both authors (SMK, PR) contributed equally to the writing of this manuscript. 2018;98:125668. During the embryological development of prefrontal areas specifically, noradrenaline plays a role in cell division, neuronal migration, differentiation as well as synaptogenesis [137,138,139,140,141].
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