Early life stress accelerates behavioral and neural maturation of the hippocampus in male mice

Early life stress (ELS) increases the risk for later cognitive and emotional dysfunction. ELS is known to truncate neural development through effects on suppressing cell birth, increasing cell death, and altering neuronal morphology, effects that have been associated with behavioral profiles indicative of precocious maturation. However, how earlier silencing of growth drives accelerated behavioral maturation has remained puzzling. Here, we test the novel hypothesis that, ELS drives a switch from growth to maturation to accelerate neural and behavioral development. To test this, we used a mouse model of ELS, fragmented maternal care, and a cross-sectional dense sampling approach focusing on hippocampus and measured effects of ELS on the ontogeny of behavioral development and biomarkers of neural maturation. Consistent with previous work, ELS was associated with an earlier developmental decline in expression of markers of cell proliferation (Ki-67) and differentiation (doublecortin). However, ELS also led to a precocious arrival of Parvalbumin-positive cells, led to an earlier switch in NMDA receptor subunit expression (marker of synaptic maturity), and was associated with an earlier rise in myelin basic protein expression (key component of the myelin sheath). In addition, in a contextual fear-conditioning task, ELS accelerated the timed developmental suppression of contextual fear. Together, these data provide support for the hypothesis that ELS serves to switch neurodevelopment from processes of growth to maturation and promotes accelerated development of some forms of emotional learning.     

BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex.

Maturation of the visual cortex is influenced by visual experience during an early postnatal period. The factors that regulate such a critical period remain unclear. We examined the maturation and plasticity of the visual cortex in transgenic mice in which the postnatal rise of brain-derived neurotrophic factor (BDNF) was accelerated. In these mice, the maturation of GABAergic innervation and inhibition was accelerated. Furthermore, the age-dependent decline of cortical long-term potentiation induced by white matter stimulation, a form of synaptic plasticity sensitive to cortical inhibition, occurred earlier. Finally, transgenic mice showed a precocious development of visual acuity and an earlier termination of the critical period for ocular dominance plasticity. We propose that BDNF promotes the maturation of cortical inhibition during early postnatal life, thereby regulating the critical period for visual cortical plasticity.     

Comparative development in Moenkhausia pittieri and Paracheirodon innesi (Ostariophysi: Characiformes) with comments on heterochrony and miniaturization in the Characidae

Developmental heterochronies between the small‐sized Moenkhausia pittieri and the miniature Paracheirodon innesi were determined by describing and comparing external morphological development in both species. Despite being classified as miniature, P. innesi was larger and more developed in the flexion and post‐flexion larval stages than M. pittieri. Broader patterns within the Characidae suggest that body size reduction in P. innesi is tied to accelerated development and higher growth rate along with early maturation and precocious cessation of growth, which are characteristic of miniature species. Comments on adipose‐fin loss in Characidae as a consequence of developmental truncation are included.     

Effects of photoperiod on sexual maturation and somatic growth in male Atlantic halibut (Hippoglossus hippoglossus L.)

A major obstacle in modern, intensive aquaculture is the precocious maturation of male fish, leading to decreased somatic growth and reduced filet quality. Effects of photoperiod on sexual maturation and growth in male Atlantic halibut were therefore examined. In June 1996, 1300 1+ fish of both sexes were distributed in two indoor tanks supplied with continuous light (LL) or a simulated natural photoperiod (SNP). In December 1996 and June 1997, 200 individuals were exchanged between the tanks creating six experimental groups that were followed until June 1998. LL stimulated growth and accelerated timing of first maturation by approximately 3 months. LL also appeared to interrupt circannual rhythmicity in sexual maturation. Sexual maturation led to reduced growth from 3 months pre-spawning and throughout the spawning season. Males that did not mature during the experiment attained the highest final body weight. All males reared on LL from June 1997 reached sexual maturity the following season. In contrast, only 26% of the males matured in the group transferred from LL to SNP in June 1997, and this group also had the highest final body weight. The results indicate a possible route for reducing the problem of precocious maturation in male halibut.     

Precocious testicular growth in metamorphosis-arrested larvae of a salamander Hynobius retardatus: role of thyroid-stimulating hormone

Precocious maturation of testes occurs in goitrogen-treated larvae of a salamander Hynobius retardatus, a particular population of which has been reported to show a neotenic reproduction in a specific environment. Similar precocious growth of testes also was confirmed in thyroidectomized larvae in this study. A possible involvement of thyroid-stimulating hormone (TSH) in the precocious maturation of testes was examined in metamorphosis-arrested larvae whose thyroid or pituitary glands had been removed surgically at embryonic stages or which had been reared in goitrogens. The pituitary glands of both the thyroidectomized and goitrogen-treated larvae contained extraordinarily large number of TSH cells, which were called "thyroidectomy cells." When homogenates of the pituitary glands from the goitrogen-treated larvae were injected into the hypophysectomized larvae for a month, the testes grew larger than those in larvae injected with the pituitary glands from normally metamorphosed controls. These results are consistent with the idea that an extraordinarily high concentration of TSH, which is induced by either thyroidectomy or goitrogen-treatment, causes the precocious maturation of testes in the metamorphosis-arrested larvae of Hynobius retardatus. In contrast to the precocious testicular development, ovarian development in the metamorphosis-arrested larvae was almost identical to that in normally metamorphosed animals within our experimental period. This also suggests that in males the absence of thyroid hormones allows a gonadal response that in females may require another activator in addition to or following thyroid axis stimulation.     

Seed Development in Phaseolus vulgaris L. cv Seminole: II. Precocious Germination in Late Maturation

Seeds of Phaseolus vulgaris L. cv Seminole in late maturation phase germinated precociously in vitro. Germination occurred in the absence of free water after 5 days but within 24 to 48 hours in contact with water. Excised axes germinated within 12 hours and embryos by 48 hours only if supplied with water. Ethylene accelerated the germination of seeds and embryos irrespective of water availability. There was no effect of ethylene on the rate of axis germination. Ethylene was equally effective within the range 0.5 to 1000 parts per million and 1 hour exposure was fully effective. Induction of precocious germination in vivo was observed by manipulating water content inside pods or by ethylene injection, whether pods were attached to the parent plant or not. These results demonstrate the importance of endogenous regulation of water supply in suppressing precocious germination. Ethylene is identified as a powerful antagonist to the natural control.     

Body size versus gonad maturation form in under-yearling precocious males of the sea trout (Salmo trutta m. trutta L.)

The study was aimed at analysing body size in relation to form of gonad maturation (amount of mature germ cells) in 329 under-yearling sea trout males. The fish, aged 7 months, were caught in late October-early November in 3 streams located in north-western Poland. Each stream supported fish belonging to a different sib group. Standard histological techniques and a computer image analysis programme were used to detect the class of gonad maturation and percentage of the gonad area occupied by tubules with active spermatogenesis. Gonad maturation forms were distinguished based on the latter criteria. Gonads with developing germ cells occupying less than 90% of gonad area were classified as incomplete forms of gonad maturation, others as complete maturation forms. In each sib-groups analysed, even the smallest individual were already precocious, their gonads being incompletely mature. The smallest maturing male measured 7.1 cm in length. The average size of an incompletely maturing individual was slightly smaller than that of the completely mature one but the difference lacked statistical significance (P > 0.05). The sib-group of smaller fish contained less precocious, and the gonads of the more precocious were incompletely mature, compared to the sib-group of larger fish (P < 0.001). It seems that the incomplete form of gonad maturation (defected maturation) occurs at a smaller critical fish size than the complete gonad maturation form. Incomplete maturation is more frequent smaller individuals and possibly in among slow-growing groups of fish.     

Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken

Both the Weybridge strain and a mixture of six laboratory and field strains of Eimeria maxima have been attenuated by selection for early maturation of oocysts during serial passage in chickens. The prepatent times of the resultant precocious lines produces after selection were reduced from approximately 120 hr to less than 107 hr, and their reproduction and pathogenicity were less than those of the parent strains. Chickens which had been inoculated with a small number of oocysts of the Weybridge precocious or mixed field isolate precocious lines were immune to subsequent challenge with the parent strains. In a comparison made between the endogenous development of the precocious lines and their parent strains, it was found that asexual multiplication of the precocious lines was reduced, due to the earlier onset of gametogony. The results of this study also indicate that the parent (i.e., normal) strains of E. maxima probably undergo a minimum of four generations of schizogony.     

Sexual behaviour of immature male eastern mosquitofish: a way to measure intensity of intra-sexual selection?

Immature males of eastern mosquitofish Gambusia holbrooki start to be sexually active well before their copulatory organ (gonopodium) has completely developed and before they become able to transfer sperm. Sexual activity of males, consisting of copulatory attempts tending to bypass female acceptance, is intense (one attempt per minute) and is likely to be energetically very costly. The sexual behaviour of immature males relative to their maturation stage is described and tested against two possible adaptive explanations. Sexual activity was present in males from the beginning of the development of their gonopodium and increased during the following stages of maturation. Two to three weeks before gonopodium development was completed, sexual activity of immatures was as high as that of adults. Adult males showed aggressive behaviour against a male attempting a copulation, irrespective of the maturity of the latter. Since previous studies have shown that the reproductive success in this species is negatively correlated with male size when male–male competition is low (i.e. when the sex ratio is female biased), but decreases with male size when competition is high, the hypothesis was tested that sexual activity of immature males functions as a way to predict their future reproductive success if they mature at a given size. A second hypothesis tested was that precocious sexual experience improves the efficiency of copulatory attempts. Results were more in agreement with the first hypothesis, since size at maturity of males was influenced by the sex ratio experienced during maturation and precocious experience gave very little advantage.     

Protein Synthesis during Natural and Precocious Soybean Seed (Glycine max [L.] Merr.) Maturation

Protein synthesis was studied during precocious and natural soybean seed (Glycine max [L.] Merr.) maturation. Developing seeds harvested 35 days after flowering were precociously matured through controlled dehydration. Total soluble proteins and proteins labeled with [³⁵S]methionine were extracted from control, developing seeds and from precociously and naturally matured seeds and were analyzed by one-dimensional PAGE and fluorography. The results demonstrated that several polypeptides which were designated “mature polypeptides,” were synthesized de novo during precocious and natural seed maturation. Two of these polypeptides, 31 and 128 kilodalton in mass, also stained intensely with Coomassie blue, suggesting their abundant accumulation during seed maturation. Results from in vitro translation experiments showed that the mRNAs corresponding to these “maturation polypeptides” accumulated during precocious maturation and in naturally matured seeds, but not in seeds freshly harvested 35 days after flowering (control). The role of the “maturation polypeptides” is currently unknown; however, their presence and that of their corresponding mRNAs was coincident with the ability of matured seeds to establish seedling growth. This study has demonstrated that precocious seed maturation treatments may be extremely useful for investigations of metabolic events and molecular control mechanisms affecting soybean seed maturation.     

A comparative study of the performance of family groups of Atlantic salmon reared in tanks and released in a river

A study was conducted in in the Dale River as a part of a stock enhancement programme. The aim was to compare growth and the incidence of precocious maturation between offspring from precocious and large maturing males, and to study genotype‐environment interactions. River and hatchery performance was compared for 5 × 2 maternal half‐sib family groups, which were stocked as 0+ juveniles or maintained in the hatchery throughout. To identify the offspring, the broodfish were characterized by DNA‐fingerprinting (eight microsatellite markers). Smolt size of 1+ hatchery‐reared smolt and fish caught in a smolt trap, and the size and incidence of precocious maturation among 1+ hatchery‐reared parr and 1+ and 2+ parr caught in the river are compared between the families.     

Life‐history traits of the common pandora Pagellus erythrinus L., interpreted using information from aquaculture experiments

A study was conducted in in the Dale River as a part of a stock enhancement programme. The aim was to compare growth and the incidence of precocious maturation between offspring from precocious and large maturing males, and to study genotype‐environment interactions. River and hatchery performance was compared for 5 × 2 maternal half‐sib family groups, which were stocked as 0+ juveniles or maintained in the hatchery throughout. To identify the offspring, the broodfish were characterized by DNA‐fingerprinting (eight microsatellite markers). Smolt size of 1+ hatchery‐reared smolt and fish caught in a smolt trap, and the size and incidence of precocious maturation among 1+ hatchery‐reared parr and 1+ and 2+ parr caught in the river are compared between the families.     

Development of imaginal competence to adipokinetic hormone in Locusta: lipid and carbohydrate levels, and glycogen phosphorylase activity in precocene-induced adultiforms

Abstract. Adipokinetic responses to injection of synthetic adipokinetic hormone I (sAKH) were investigated in precocene-induced fifth-instar adultiforms and in chemically allatectomized but morphogenetically normal adults of Locusta migratoria (L.). The results were compared with data on normal fifth (=last)-instar nymphs and normal adults. Chemical allatectomy did not affect the resting level of lipid in the haemolymph, nor the slight decrease of haemolymph carbohydrate concentration induced by sAKH. The effects of chemical allatectomy on sAKH-induced hyperlipaemia, the resting level of haemolymph carbohydrate, total glycogen phosphorylase specific activity, as well as sAKH-induced phosphorylase activation in the fat body, were mostly minor and probably indirect. The concentrations of lipid and carbohydrate in the haemolymph, and sAKH-induced activation of fat body glycogen phosphorylase were more or less similar in normal fifth-instar nymphs, normal adults and fifth-instar adultiforms. Thus, precocious metamorphosis did not affect markedly those parameters which show no or slight changes during normal metamorphosis. In contrast, parameters which change substantially during normal metamorphosis (sAKH-induced hyperlipaemia, sAKH-induced changes in haemolymph carbohydrate level and total glycogen phosphorylase activity) showed similar changes in the course of precocious metamorphosis; the values for fifth-instar adultiforms were similar to those obtained for normal adults, but differed markedly from those found in normal fifth-instar nymphs. Thus, accelerated (precocious) morphological adult development is strongly correlated with accelerated imaginal target competence to AKH and with relevant physiological development.     

Chimeric nature of precociously-germinating Brassica napus embryos: mRNA accumulation patterns

During precocious germination, Brassica napus L. embryos exhibitfeatures of embryo maturation and features of post-germinativegrowth at the same time, which raises important questions aboutthe nature of these developmental programmes and the transitionbetween them. To investigate the possiblity that the two programmesare segregated spatially rather than temporallhy in these embryos,embryos of different ages (excised at 38, 47, and 60 d post-anthesis)were placed in culture to induce precocious germination, andtotoal RNA was isolated from the cotyledons and axes or hypocotyls.cDNA sequences (two marking embryo maturation and four markingthe onset of post-germinative growth) were used as probes ondot blots to compare mRNA population dynamics in these organs.We find that individual organs accumulate mRNAs characteristicof only one developmental programme at any given time and concludethat the programmes are both distinct and potentially mutuallyexclusive. Embryos are able to ‘switch’ from accumulatingembryo maturation mRNAs to acumulating post-germinative mRNAsin culture, but the transition occurs at different times indifferent organs. Key words: Precocious germination, Brassica napus, rapeseed, embryo development     

The effect of manipulating ecdysteroid signaling on embryonic eye development in the locust<Emphasis Type="Italic"> Schistocerca americana</Emphasis>

Adult body plan differentiation in holometabolous insects depends on global induction and control by ecdysteroid hormones during the final phase of postembryogenesis. Studies in Drosophila melanogaster and Manduca sexta have shown that this pertains also to the development of the compound eye retina. It is unclear whether the hormonal control of postembryonic eye development in holometabolous insects represents evolutionary novelty or heritage from hemimetabolous insects, which develop compound eyes during embryogenesis. We therefore investigated the effect of manipulating ecdysteroid signaling in cultured embryonic eye primordia of the American desert locust Schistocerca americana, in which ecdysteroid level changes are known to induce three rounds of embryonic molt. Although at a considerably reduced rate compared to in vivo development, early differentiation and terminal maturation of the embryonic retina was observed in culture even if challenged with the ecdysteroid antagonist cucurbitacin B. Supplementing cultures with 20-hydroxyecdysone (20E) accelerated differentiation and maturation, and enhanced cell proliferation. Considering these results, and the relation between retina differentiation and ecdysteroid level changes during locust embryogenesis, we conclude that ecdysteroids are not an essential but possibly a modulatory component of embryonic retina development in S. americana. We furthermore found evidence that 20E initiated precocious epithelial morphogenesis of the posterior retinal margin indicating a more general role of ecdysteroids in insect embryogenesis.Electronic Supplementary Material Supplementary material is available in the online version of this article at Edited by C. Desplan     

Precocious floral initiation and identification of exact timing of embryo physiological maturity facilitate germination of immature seeds to truncate the lifecycle of pea

We propose herein a novel single seed descent protocol that has application across a broad phenotypic range of pea genotypes. Manipulation of key in vivo growing conditions, including light, photoperiod and temperature, combined with precocious in vitro germination of the embryo at full physiological maturity substantially shortened the pea lifecycle. We define full embryo physiological maturity as the earliest point in seed development when precocious in vitro germination and robust seedling growth can be reliably achieved without supply of exogenous hormones. Under our optimised conditions for accelerated plant growth, embryo physiological maturity was attained at c. 18 days after pollination, when seed moisture content was below 60?% and sucrose level under 100 mg g^?1 DW. No delay penalty in terms of time to flowering and plant development was caused by the culture of immature seeds 18 days after pollination compared to the used of mature ones. Determining the role embryo maturity plays in the fitness of the germinated plant has facilitated the truncation of the lifecycle across pea genotypes. The accelerated single seed descent system proposed within this research will benefit complex genetic studies via the rapid development of recombinant inbred lines (RIL) and multi-parental advanced generation intercrosses (MAGIC) populations.     

Precocious development of sympatho-adrenal function in rats whose mothers received methadone

The development of the ability of insulin-induced hypoglycemia to cause reflex neuronally-mediated release of adrenal catecholamines was studied in rats exposed perinatally to methadone. In control rats, the response was absent at birth and developed by the first week of postnatal age. Rats whose mothers received daily injections of methadone showed precocious development of neonatal sympatho-adrenal responses, an effect which reflected earlier maturation of functional sympathetic innervation of the tissue. The developmental alteration caused by methadone was apparent even in rats withdrawn from drug at birth by cross-fostering to normal mothers; the effect also did not display a “critical period,” in that prenatal exposure alone produced the shift as well as did continuous exposure. Accelerated maturation of sympatho-adrenal function caused by methadone appeared to be independent of nutritional or body weight factors, and may represent a direct drug effect on the fetus or pup.     

Genetic Deletion of NR3A Accelerates Glutamatergic Synapse Maturation

Glutamatergic synapse maturation is critically dependent upon activation of NMDA-type glutamate receptors (NMDARs); however, the contributions of NR3A subunit-containing NMDARs to this process have only begun to be considered. Here we characterized the expression of NR3A in the developing mouse forebrain and examined the consequences of NR3A deletion on excitatory synapse maturation. We found that NR3A is expressed in many subcellular compartments, and during early development, NR3A subunits are particularly concentrated in the postsynaptic density (PSD). NR3A levels dramatically decline with age and are no longer enriched at PSDs in juveniles and adults. Genetic deletion of NR3A accelerates glutamatergic synaptic transmission, as measured by AMPAR-mediated postsynaptic currents recorded in hippocampal CA1. Consistent with the functional observations, we observed that the deletion of NR3A accelerated the expression of the glutamate receptor subunits NR1, NR2A, and GluR1 in the PSD in postnatal day (P) 8 mice. These data support the idea that glutamate receptors concentrate at synapses earlier in NR3A-knockout (NR3A-KO) mice. The precocious maturation of both AMPAR function and glutamate receptor expression are transient in NR3A-KO mice, as AMPAR currents and glutamate receptor protein levels are similar in NR3A-KO and wildtype mice by P16, an age when endogenous NR3A levels are normally declining. Taken together, our data support a model whereby NR3A negatively regulates the developmental stabilization of glutamate receptors involved in excitatory neurotransmission, synaptogenesis, and spine growth.     

Changes in Seed Constituents During Germination and Seedling Growth of Precociously Matured Soybean Seeds(Glycine max)

During 7 d of precocious maturation of soybean seed (Glycinemax), the starch content declined and soluble sugar levels increasedin patterns similar to natural seed dehydration and maturation.Total seed protein content and total seed dry weight increasedwhereas oil content remained relatively unchanged. Overall,the proportions of the constituents in precociously maturedseeds were comparable to naturally mature seeds. Precociouslymatured soybean seeds showed much the same germination and seedlinggrowth frequency patterns as naturally matured seeds. Duringgermination and seedling growth of precociously matured seeds,starch, soluble sugar, protein and oil levels followed patternssimilar to naturally mature, germinating seeds and seedlings.Therefore, precocious maturation may be used as a model systemto investigate the control of the physiological and biochemicalevents occurring during seed maturation which lead to germinationand subsequently, seedling growth. Glycine max (L.) Merr., soybean, cotyledons, maturation, germination/seedling growth