Hence, adolescence represents a second stage in the development of CNS where steroid hormones, increasing during puberty, trigger permanent structural changes. Organizational effects are explained through changes occurring in the CNS due to five mechanisms: Influence of sex steroids on the organizational and activational effects that shape the adolescent brain.
Organizational effects such as epigenetic mechanisms, neuronal and receptor pruning, remodeling of dendritic spines, myelination, and apoptosis are common during adolescence. These effects lead to the maturation and remodeling of cortical and limbic circuits, a fact that favors the expression of certain behaviors in adulthood, if activational effects occur. This is the process of forming a myelin sheath around the neuron axon.
Myelin confers on axons their characteristic white appearance, and thus myelination is responsible for the increase in white matter in the brain during adolescence Morriss et al. In the CNS, myelin is synthesized by oligodendrocytes, while in the peripheral nervous system synthesis is performed by Schwann cells Curry and Heim In males, testosterone is fundamental in myelination since its administration seems to partly induce maturation of oligodendrocytes and formation of myelin Kafitz et al.
In females, on the other hand, estradiol and progesterone facilitate myelination, inducing the synthesis of myelin basic protein Jung-Testas et al. The relevance of an adequate myelination process, therefore, lies in the fact that the development of the myelin sheath enhances the flow of information along the axons, and thus, leads to a faster and more efficient processing of information Spear a.
Dayan and Guillery-Girard state that the development of white fibers resulting from myelination increases exponentially during adolescence, a process comparable to the resumption of the development tendencies observed during the first 5 years of life.
Neuronal pruning or synaptic pruning refers to the decrease in synaptic density decrease in the number of synapses per unit of brain tissue Luna which had increased during the process of synaptogenesis during the individual's early development. In the prepuberal stage, the volume of gray matter increases significantly i. During neural pruning, frequently used synaptic connections are reinforced and conserved, while seldom activated synapses degenerate.
Hence, nerve circuits acquire a much more efficient synaptic configuration. In other words, neural pruning eliminates unwanted connections and solidifies brain circuitry Ruben and Caskey Synaptic pruning is then a neural mechanism reflecting the elimination of the least active synapses, explaining the decrease of gray matter in adolescence Weiten Neuronal pruning takes place, for example, in students with good bodily-kinesthetic skills who are not encouraged to move or exercise Teele Apoptosis programed cell death and other types of cell death allow for variation in the volume of different brain regions; they constitute mechanisms of neural plasticity and operate mainly in the embryonic stage.
In fact, the developing nervous system produces more new neurons than are actually used, and selective pruning occurs by apoptosis Gore et al. Estradiol shows a dual effect in this process: In effect, one of the first nuclei showing sexual dimorphism a concept to be discussed later was identified in the preoptic area, and it is several times bigger in male than in female rats; such dimorphism is partially caused by steroid hormones on the apoptopic processes at play during brain development Gore et al. Dendritic spines, the small cytoplasmic extensions where synapses occur Diamond, Gray, and Yasargil , cover neuronal dendrites.
These structures constitute a quite dynamic type of dendrite they grow, persist, or degenerate according to the stimuli they receive , so each dendrite has a different spine remodeling, which can be altered by endocrine-metabolic pathologies, steroid hormone fluctuations, and ageing, among others Coke and Wolley , as well as by other exogenous elements such as drugs, synthetic hormones, and their derivatives. Among adult female rats, dendritic spine density changes along the normal ovarian cycle, being higher in the proestrus than in the estrus and diestrus Chen et al.
This indicates that estradiol could also promote dendritic spine formation and remodeling in other species such as humans. Some of the changes observed in the adolescent brain are believed to be controlled by epigenetic phenomena, regulated in different ways by sex steroid hormones.
Epigenetic changes allow for modifications in the expression of certain genes and, thus, changes in brain structures or even in behavior and are manifested through the following mechanisms: DNA methylation has been linked to a decrease in the expression of estrogen and progesterone receptors in some brain regions known to undergo changes during puberty Prewitt and Wilson ; Westberry, Trout, and Wilson In castrated murine models, alterations are observed in the methylation patterns in the anteroventral and periventricular nucleus, which can be reverted by injecting testosterone.
The expression of kiss1 , the kisspeptin encoding-gene, has proved to be epigenetically regulated by DNA methylation. An alteration in the gene methylation can lead to an early onset of the rat fertile cycle Lomniczi et al.
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Brain histone acetylation changes when exposed to sex steroids, while inhibition of acetylation leads to a series of changes in reproductive behavior. In addition, a dimorphism concept discussed later may be observed in acetylation patterns, which could explain certain differences between the sexes Morrison et al. Brain microRNA micro milieu changes in response to sex steroids and has a completely different pattern in males and females once puberty begins. This mechanism could exert a relevant role in the sexual dimorphisms developed during adolescence and puberty Morrison et al.
Sexual dimorphism is defined as the set of differences in the anatomic and physiological attributes of males and females of the same species, e. The female and male brains are known to be physically and biologically distinct. Current evidence suggests that most of these differences originate during adolescence due to changes triggered by the amount of female and male sex steroids released, which vary from puberty onwards.
There is higher intrahemispheric connection in men, which could be associated to a higher coordination between perception and execution. On the other hand, women evidence increased interhemispheric connectivity, which could relate to a more efficient communication between analytic and intuitive processing. The male brain is predominantly hard-wired for understanding and building systems.
Results suggest that this stage of development presents morphological changes in the brain associated to hormone levels. Men show correlation between high testosterone levels and lower volume of gray matter in the anterior singular cortex; women, however, show no change from childhood to adolescence in this region, which is linked to the assessment of options before taking action. On the other hand, women who were found to possess high testosterone levels had a higher volume of gray matter in the frontal orbital cortex, a fact exerting a major influence on decision making both when risk is involved and when decisions are based on assessment of rewards.
In order to determine to what extent changes in the adolescent brain are dependent on hormones, Herting et al. Results show that, regardless of age, variations in cortical volume and in some subcortical regions such as the amygdala and caudate relate to the levels of testosterone and estradiol Herting et al. The sexual dimorphisms found are not only structural, but also cognitive and functional.
Such distinction corresponds to differences in estrogen levels. This would explain the distinctive emotional circuits of men and women. Some neuroimaging studies suggest the existence of a series of activational effects in the amygdala and prefrontal cortex; in fact, both show higher sexual dimorphism during puberty and adolescence because of their dissimilar levels of gonadal hormones. Such effects would partially explain the differences in emotion and affection between both sexes Van Wingen et al.
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Some decades ago, it was generally agreed that brain organizational changes took place only during embryonic development, while activational changes hormone-regulated occurred during puberty. However, both types of changes have been subsequently associated with puberty and adolescence Schulz et al.
Research assessing copulatory behavior in the male hamster in the presence of a female hamster has provided relevant information in this respect Schulz et al. In these experiments, the prepuberal rodents who were administered testosterone did not copulate. The same happened with adult males under the same conditions, but castrated in the prepuberal stage. However, adult hamster males who had been castrated during their postpuberal stage immediately generated copulatory responses following testosterone administration.
Thus, copulatory response in adult rodents requires the presence of testosterone both in puberty and in adulthood Schulz et al. Therefore, this behavior results from a hormonal effect at an activational level. The behavior, however, only occurs provided there has been a previous organizational change triggered by exposure to testosterone in puberty; the latter coordinates the neural circuitry required to exhibit the characteristic adult sexual behavior in the presence of sex steroid hormones and a female individual.
The proof that such organizational events did not take place during the embryonic stage lies in that hamsters did not show sexual behavior under the same circumstances in the prepuberal period Schulz et al. Copulatory behavior was only evidenced in adults given that, in their puberal stage, they possessed gonads able to secrete physiological concentrations of sex steroid hormones.
This suggests that certain organizational processes occur during adolescence. The effect of androgens, such as testosterone and dihydrotestosterone, is strong from the embryonic and fetal periods. In addition, androgens can affect cognitive abilities. A classic study on verbal and spatial ability tests conducted on men by Hier and Crowley showed no differences in verbal skills, but lower scores in subjects with prepuberal idiopathic hypogonadism and postpuberal hypogonadism, as compared to control.
Androgen replacement therapy through administration of testosterone after puberty did not affect the scores of either hypogonadic group Hier and Crowley The latter suggests that organizational changes determining the development of spatial skills are also activated during adolescence, which requires physiological levels of androgens testosterone or its derived metabolites produced by functional gonads.
The effect of steroid hormones in the process results, in the first place, from their interaction with their receptors in the neurons, and, next, from the coordination and execution of specific cell responses. This phenomenon can be better understood by studying the intracellular signaling pathways used by sex steroids, both genomic effects also known as canonical , in which hormonal action involves genetic transcription Jensen and DeSombre ; Sherman, Corvol, and O'Malley , and non-genomic non-canonical effects, where membrane receptors act through secondary messengers such as calcium cation, inositol triphosphate, cyclic adenosine monophosphate and diacylglycerol, among others Falkenstein and Wehling Extense research is currently underway to determine which steroidal effects are genomic, non-genomic, or result from a combination of both.
Interestingly, spermatozoa constitute an excellent model to study such effects Luconi et al. During its development, this cell loses its gene transcription ability; therefore, non-genomic signaling pathways are the only ones available. The fact that steroid hormone receptors in both spermatozoa and neurons are uncommonly alike in mammals represents another advantage, suggesting that both cell types possess a similar capacity to react to the same environmental hormone changes Meizel , for example, showing comparable responses to the interactions between steroid hormones and the GABAergic system Vigil et al.
GABA together with progesterone neuroactive steroid would influence mood swings in women undergoing hormone replacement therapy by inducing a negative mood Andreen et al. Estradiol, on the other hand, would present the opposite effect together with GABA, both at the CNS and in spermatozoa, leading to a state of euthymia and inhibiting AR, respectively Andreen et al. It seems reasonable to assume that in puberty changes in sex steroid levels possess a relevant role, since they not only exert their influence on the reproductive system, but would also impact brain development and organization during this stage.
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In the adolescence, steroid hormones also play a part in brain organizational development through the mechanisms of plasticity aforementioned. Thus, puberty and adolescence appear to be closely linked, considering that the brain constitutes a target organ that responds to the presence of a number of hormones whose concentration increases during puberty. To date, solid evidence suggests that gonadal hormones have a different influence on the socio-sexual behavior of men and women during adolescence Sisk Thus, during male adolescent development, testosterone programs the ability to make behavioral adaptations to social experience that improve reproductive efficience and avoid aggression, leading to better reproductive fitness.
High levels of ovarian hormones during puberty, on the other hand, seem to organize fertility-related behaviors, which is contingent on metabolic signals predicting sufficient energy availability to sustain pregnancy, lactation, and maternal care Sisk The understanding of the effects of sex steroids on behavior is still limited; however, there seems to be a correlation between the presence of endocrine disorders and certain behavioral alterations. During adolescence, sex steroids modify the structure of neuronal connections and the number of neurotransmitter receptors present in neurons since the prenatal period Weiner, Primeau, and Ehrmann Such changes would affect the CNS ability to respond to exogenous and endogenous variables, leading to affective and mood disorders Goel and Bale ; Weiner, Primeau, and Ehrmann Studies have validated this hypothesis, showing the link between free testosterone and other steroids and both premenstrual syndrome and depression in women Baischer et al.
PCOS women show high correlation between their abnormal androgen levels and mood disorders, which range from emotional problems to sexual identity problems and depression Ghaziuddin ; Orenstein et al. Fontecilla and Worthington used the Rorschach test with PCOS women, evidencing distortions in the configuration of the psychological self: Prolactin, the peptid hormone released by the adenohypophysis pituitary anterior lobe , would also modulate human mood. An interesting study by Reavley et al.
The Hospital Anxiety and Depression questionnaire was used with both groups. As a result, 54 percent hyperprolactinemia patients showed defined or borderline anxiety as compared to 27 percent of the normoprolactinemia control group. These results evidence significant presence of anxiety among a proportion of women suffering from hyperprolactinemia. On the other hand, an interesting study carried out by Lee et al.
Higher doses, however, may suppress production of the sex steroids estradiol and progesterone. Most investigations evidence that toxic stress can have an adverse effect on brain architecture. During the sensitive stages of brain development, toxic stress can produce an excessive amount of neuronal connections in the brain regions involved in fear, anxiety, and impulse responses; at the same time, it can reduce the number of neuronal connections in the areas devoted to reasoning, planning, and behavioral control NSCDC Extreme exposure to toxic stress can even alter the stress system to respond at lower thresholds to events other people would not see as stressful, and thus, more frequently and for a longer period than necessary.
Such wearing of the system increases the risk of stress-related physical and mental illnesses in adulthood NSCDC Adolescence is a stage when response to sex hormones and stress is enhanced; the maturation of dopaminergic neuronal circuits is deeply influenced by these factors Sinclair et al. In youngsters exposed to stress, increased production and secretion of glucocorticoids like cortisol partly contribute to the modern diathesis-stress hypothesis which suggests that cortisol secretion would exert a significant pathophysiological role in the etiology of depression Gillespie and Nemeroff Testosterone, estrogens, and glucocorticoids interact, having different region-specific impacts on the dopaminergic neurotransmission in the adolescent brain, shaping brain maturation, and cognitive function in adolescence and adulthood.
A marked decrease in the density of dopamine receptors by a process of receptor pruning in male rats during the periadolescent period has been reported Andersen et al. For this and other reasons, sex and stress hormones constitute easy targets for future strategies aiming at prevention and treatment of psychiatric disorders Sinclair et al. In the past few years, research has contributed significant evidence on the effect exerted by the active compounds of hormone-based contraceptives ethinyl estradiol and progestins, as well as chemically related compounds on brain excitability, and thus on the mood of the users Gingnell et al.
Even though hormonal contraceptives are among the most widely studied drugs in the history of medicine, Cobey and Buunk argue that little research has focused on determining the consequences of these drugs on female psychological welfare; this has led to users and health professionals being misinformed regarding the consequences of their use. For decades, hormonal contraceptives such as oral formulations have been thought to produce psychological disorders in female users, e.
This appears to be especially relevant considering that many adolescents are currently being prescribed such hormone formulations as contraceptive methods Feldman An interesting study of female university students 18—35 years old carried out by Nielsen et al. Considering that the effects of stress hormones e. In addition, other investigations show that the use of contraceptives by adult users affects performance in numerical cognitive tests, presenting masculinized answers Pletzer et al.
The same researcher tested androgenic and anti-androgenic contraceptives, obtaining different results for both types of drugs. The strongest changes both in structure and performance in the face recognition test were evidenced in users of androgenic contraceptives such as levonorgestrel Pletzer, Kronbichler, and Kerschbaum Another interesting observation was made by Abler et al.
The question arises whether the changes resulting from steroidal contraceptive use add their effects and risks to other noxious exogenous factors like sleep deprivation and consumption of drugs such as nicotine and alcohol, common behaviors among some adolescent girls. Together, the latter would affect the organizational processes in the brain during the adolescence, resulting in behavioral and psycho-affective disorders in the adulthood Baischer et al.
Adolescent behavior is characterized by irrational decisions, impulsivity and lack of emotional control, evidencing a particular neurological phase. Two relevant events take place at this stage: Both events are closely linked due to the physiological level of steroid hormones in adolescence, which allow for a timely and adequate remodeling of the brain circuits, determining the existence of activational effects in adulthood.
Several adult behavioral patterns, such as copulatory sexual conduct and spatial ability, are dependent upon this endocrine modulation. A number of neural plasticity mechanisms have been described through which sex steroids exert organizational changes in the brain: It is of utmost importance to consider the effects of internal and external factors capable of altering the hormonal balance during adolescence, and therefore, interfering with such plasticity mechanisms.
These could negatively influence CNS organizational modifications, triggering permanent effects which would become evidence later in adulthood, such as some endocrine-metabolic disturbances, for example, PCOS. In the face of studies evidencing that hormonal contraceptives can cause psychological disorders in women, it is important to consider these facts in under-age users of hormonal contraceptives, specifically in teenage girls whose brains are undergoing a process of remodeling by the action of sex steroids. As a way of example, the human prefrontal cortex is an area whose final volume is not reached until the early twenties Yurgelun-Todd , hence, the use of contraceptives before this age could lead to changes in this region's permanent circuitry Pletzer and Kerschbaum The latter has several implications, both from an ethical point of view and from the perspective of pediatric medicine.
Parra argues that every professional is morally obliged to properly inform the patient; in fact, patients are legally entitled to be informed. In addition, biomedical researchers, health educators e. In view of the aforementioned facts, during adolescence there is a unique plasticity window, strongly influenced by endogenous and exogenous steroid hormones, among other factors.
The effect produced by these hormones over this plasticity window is directly associated with patterns of emotional behavior in adult life. National Center for Biotechnology Information , U. Journal List Linacre Q v. Author information Copyright and License information Disclaimer. This article has been cited by other articles in PMC. Abstract This review explains the main effects exerted by sex steroids and other hormones on the adolescent brain.
Activational effects, Adolescence, Adolescent behavior, Brain development, Contraceptive steroids, Hormones, Sex steroids, Organizational effects, Puberty.
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Introduction The physical changes experienced during adolescence are remarkable and, most of them evident, especially those leading to the manifestation of secondary sex characters and contributing to the differentiation between male and female phenotype, as well as the acquisition of human reproductive capacity.
Search for Bibliographic Information Articles were searched for in the following bibliographic databases: Characteristics of the Adolescent Brain In general terms, the brain of adolescents is characterized by incomplete development of the encephalic functions determining endogenous voluntary behavior; this limits the ability to recognize erroneous information, sustain voluntary control, and become interested and motivated on the basis of future rewards. Neural Plasticity and Activational and Organizational Effects As mentioned above, brain development constitutes an ongoing process Spear a and hence the importance of neural plasticity.
Open in a separate window. Myelination This is the process of forming a myelin sheath around the neuron axon. Neuronal Pruning Neuronal pruning or synaptic pruning refers to the decrease in synaptic density decrease in the number of synapses per unit of brain tissue Luna which had increased during the process of synaptogenesis during the individual's early development.
Apoptosis Apoptosis programed cell death and other types of cell death allow for variation in the volume of different brain regions; they constitute mechanisms of neural plasticity and operate mainly in the embryonic stage. Dendritic Spine Remodeling Dendritic spines, the small cytoplasmic extensions where synapses occur Diamond, Gray, and Yasargil , cover neuronal dendrites. Epigenetic Control of Gene Expression Some of the changes observed in the adolescent brain are believed to be controlled by epigenetic phenomena, regulated in different ways by sex steroid hormones.
Sexual Dimorphism in the Adolescent Brain Sexual dimorphism is defined as the set of differences in the anatomic and physiological attributes of males and females of the same species, e. Brain Developmental Window Some decades ago, it was generally agreed that brain organizational changes took place only during embryonic development, while activational changes hormone-regulated occurred during puberty. Psychological Alterations Associated with Endocrine Disorders The understanding of the effects of sex steroids on behavior is still limited; however, there seems to be a correlation between the presence of endocrine disorders and certain behavioral alterations.
Concluding Remarks Adolescent behavior is characterized by irrational decisions, impulsivity and lack of emotional control, evidencing a particular neurological phase.
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