Human fetal hippocampal development: II. The neuronal cytoskeleton

Arnold, Steven E.; Trojanowski, John Q.

doi:10.1002/(sici)1096-9861(19960401)367:2<293::aid-cne10>3.0.co;2-s

Cited by 85 publications

(42 citation statements)

References 60 publications

(38 reference statements)

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“…Although hippocampal cytoarchitecture is well established by 34 weeks of gestation, 61,62 neuronal proliferation and myelination continue through adolescence, both in rodents and primates. 58,61 In a large postmortem brain sample, Benes 63 observed increased myelination of the subicular and presubicular regions during the late adolescent period.…”

Section: Discussionmentioning

confidence: 98%

Three-Dimensional Mapping of Hippocampal Anatomy in Adolescents With Bipolar Disorder

Bearden

Soares

Klunder

et al. 2008

Journal of the American Academy of Child & Adolescent Psych

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Objective-Early-onset bipolar disorder is thought to be a particularly severe variant of the illness. Continuity with the adult form of illness remains unresolved, but preliminary evidence suggests similar biological underpinnings. Recently, we observed localized hippocampal decreases in unmedicated adults with bipolar disorder that were not detectable with conventional volumetric measures. Using the same three-dimensional mapping methods, we sought to investigate whether a similar pattern exists in adolescents with bipolar disorder.Method-High-resolution brain magnetic resonance images were acquired from 16 adolescents meeting DSM-IV criteria for bipolar disorder (mean age 15.5 ± 3.4 years, 50% female) and 20 demographically matched, typically developing control subjects. Three-dimensional parametric mesh models of the hippocampus were created from manual tracings of the hippocampal formation.Results-Controlling for total brain volume, total hippocampal volume was significantly smaller in adolescent patients with bipolar disorder relative to controls (by 9.2%). Statistical mapping results, confirmed by permutation testing, revealed significant localized deformations in the head and tail of the left hippocampus in adolescents with bipolar disorder, relative to normal controls. In addition, there was a significant positive correlation between hippocampal size and age in patients with bipolar disorder, whereas healthy controls showed an inverse relation.Discussion-Localized hippocampal deficits in adolescent patients with bipolar disorder suggest a possible neural correlate for memory deficits observed in this illness. Moreover, age-related increases in hippocampal size in patients with bipolar disorder, not observed in healthy controls, may reflect abnormal developmental mechanisms in bipolar disorder. This possibility must be confirmed by longitudinal studies.Correspondence to Dr. Carrie E. Bearden, Department of Psychiatry and Biobehavioral Sciences, UCLA, 300 Building Medical Plaza, Suite 2265, Los Angeles, CA 90095; e-mail: cbearden@mednet.ucla.edu. This article is the subject of an editorial by Dr. Hilary P. Blumberg in this issue.Disclosure: Dr. Birmaher has participated in forums sponsored by Solvay Pharmaceuticals and Abcomm, and has received royalties from Random House.The other authors report no conflicts of interest. Much less is known about the neurobiological underpinnings of juvenile-onset bipolar disorder, although it is thought to be a particularly severe variant of the illness, 9,10 potentially with a higher genetic loading. 11 Its continuity with the adult form of the illness remains unresolved, but neuroanatomical findings to date in early-onset bipolar disorder appear similar to those for adults, with most studies finding no differences in global hippocampal volume between children with bipolar disorder and controls. [12][13][14] In contrast, two studies have identified hippocampal volume decreases in young patients with bipolar disorder. 15,16 In particular, in a sample of adolescents...

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Section: Discussionmentioning

confidence: 98%

Three-Dimensional Mapping of Hippocampal Anatomy in Adolescents With Bipolar Disorder

Bearden

Soares

Klunder

et al. 2008

Journal of the American Academy of Child & Adolescent Psych

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“…Studies in humans have emphasised the importance of the maternal TH environment prior to the onset of fetal thyroid function (18-20 weeks gestation in humans) with respect to fetal brain development (Connolly & Pharoah 1989, Pop et al 1999). -Internexin, NF-L and GFAP are expressed in human fetal brain from at least 9 weeks gestation (Voronina & Preobrazhensky 1994, Arnold & Trojanowski 1996. Thus, similar compromise to that seen in the rat may contribute to the cognitive and motor dysfunction seen in the offspring of hypothyroid women (Connolly & Pharoah 1989, Man et al 1991, Haddow et al 1999.…”

Section: Discussionmentioning

confidence: 99%

Maternal thyroid status regulates the expression of neuronal and astrocytic cytoskeletal proteins in the fetal brain

Sampson

Pickard²,

Sinha³

et al. 2000

Journal of Endocrinology

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Maternal thyroid hormone (TH) crosses the placenta and is postulated to regulate fetal brain development. However, TH-dependent stages of fetal brain development remain to be characterised. We have therefore compared the levels of several neuronal and glial cytoskeletal proteins in fetal brains from normal (N) and partially thyroidectomised (TX) rat dams by immunoblotting. Pregnancies were studied both before and after the onset of fetal TH secretion, which occurs at 17·5 days gestation (dg) in the rat.Maternal hypothyroidism disrupted fetal growth, so that fetal body and brain weights were reduced near term. Vimentin expression was unaffected, however, indicating normal acquisition of neuronal and glial precursor cells. Fetal brain levels of glial fibrillary acidic protein (GFAP) were reduced at 21 dg, suggesting delayed astrocytic differentiation, although regression analysis demonstrated appropriate GFAP levels for brain weight. Levels of -internexin, the earliest neurofilament protein expressed in fetal brain were reduced at 16 dg in TX dams, but increased at 21 dg. The ontogeny of neurofilament-L was also perturbed in these pregnancies, with deficient levels apparent at both 16 and 21 dg. These effects on neuronal cytoskeletal proteins were unrelated to fetal brain growth retardation.These findings confirm that maternal hypothyroidism disrupts early fetal brain development. Early disturbances in neuronal differentiation are not corrected by the onset of fetal TH secretion. Such disturbances may contribute to the neurological damage observed in children born to hypothyroxinaemic mothers.

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“…Differentiation of the hippocampal cell fields has been shown in rodents and humans to proceed from CA1 to CA3 (Bayer and Altman 1974;Arnold and Trojanowski 1996). Maturation of the CA fields in non-human primates may follow the same pattern.…”

Section: Hippocampal Formationmentioning

confidence: 99%

Revisiting the Maturation of Medial Temporal Lobe Memory Functions in Primates

Alvarado¹,

Bachevalier²

2000

Learn. Mem.

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In a review of the literature on the development of the medial temporal lobe region in humans, monkeys, and rodents, Bachevalier and Beauregard indicated that in primates, memory functions subserved by this neural system emerge early in life and increment gradually with further postnatal maturation. Furthermore, they stated that the late-developing memory functions of normal neonates was more likely owing to the slow maturation of the association areas of the cortex than to the slow maturation of the hippocampal formation. This conclusion was based on the limited knowledge concerning the development of hippocampal-dependent memory functions and the maturational events in the medial temporal lobe of monkeys. Over the last decade, however, more information has accumulated about the structural, functional, and behavioral changes occurring throughout ontogeny in monkeys that suggest a refinement of this view. Whereas there is still much to be discovered, we thought it timely to put into perspective the latest findings in hope of shedding light on memory development in general, and particularly, on the role of medial temporal lobe structures in infant and adult memory. [Note: Hippocampal formation refers to the hippocampus proper (Ammon's fields), dentate gyrus, and subicular complex. Hippocampal region refers to the hippocampal formation and the adjacent entorhinal, perirhinal, and parahippocampal cortex.]It is generally accepted that memory is not a unitary process, but rather consists of multiple systems (for review, see Squire 1994), only one of which depends critically upon the hippocampal formation. The dissociation between these memory systems has received further support from developmental studies of memory in which it has been shown that memory processes that are sensitive to hippocampal dysfunction in adults are late developing in infants. Such findings have been particularly well documented in rodents. Because neurogenesis in the rodent dentate gyrus is almost entirely postnatal, the onset of particular behavioral events can be readily compared to maturational changes in the hippocampal formation (Altman et al. 1973;Douglas 1975). In particular, these behavioral functions emerge between ages 20 and 25 d, just at the end of neurogenesis and synaptogenesis in the dentate gyrus (Altman and Das 1965;Altman and Bayer 1975;Bayer 1980). For example, the ability to navigate to a hidden platform in a water maze or perform a delayed alternation task (Freeman and Stanton 1991) first appears at this age and is impaired in adults with damage to the hippocampal formation (Morris et al. 1982). This tight link between maturational events within the rodent hippocampal formation and associated structures and emergence of memory abilities has encouraged the extension of these comparisons to other species, including human and non-human primates.One striking difference between rodent and primate species is that the neurogenesis of the hippocampus proper and dentate gyrus in monkeys and humans is almost entirely prenatal Ecken...

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Human fetal hippocampal development: II. The neuronal cytoskeleton

Cited by 85 publications

References 60 publications

Three-Dimensional Mapping of Hippocampal Anatomy in Adolescents With Bipolar Disorder

Three-Dimensional Mapping of Hippocampal Anatomy in Adolescents With Bipolar Disorder

Maternal thyroid status regulates the expression of neuronal and astrocytic cytoskeletal proteins in the fetal brain

Revisiting the Maturation of Medial Temporal Lobe Memory Functions in Primates

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