The impact of maternal separation on the number of tyrosine hydroxylase-expressing midbrain neurons during different stages of ontogenesis

Chocyk, Agnieszka; Przyborowska, Aleksandra; Dudys, Dorota; Majcher, I.; Maćkowiak, Marzena; Wędzony, K

doi:10.1016/j.neuroscience.2011.03.008

Cited by 43 publications

(62 citation statements)

References 102 publications

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“…2005; Munro et al 2006). Gender-specific differences in the function of brain monoamine systems early trauma have previously been reported in rodents exposed to early life stress (Chocyk et al 2011; Festa et al 2004; Matthews et al 2001; Nazarian et al 2009; Walker et al 2006). Interestingly, maternal separation has been shown to be associated with ethanol consumption and preference in male, but not female rats (Gustafsson et al 2005; Jaworski et al 2005; Moffett et al 2007; Roman et al 2004).…”

Section: Discussionmentioning

confidence: 77%

“…Interestingly, there is also preclinical evidence showing that early life stress may lead to long-term derangements in DA neurotransmission that persist into adulthood. Rodents exposed to early life stress exhibit altered ventral striatal (VS) and nucleus accumbens (NAcc) DA responses to stress in later life (Brake et al 2004; Chocyk et al 2011; Fulford and Marsden. 1998; Jahng et al 2010; Meaney et al 2002; Hall et al 1999), as well as enhanced DA responses to psychostimulants (Hall et al 1999; Kosten et al 2005; Moffett et al 2006) and increased alcohol/drug consumption (Kosten et al 2005; Moffett et al 2007; Zhang et al 2005).…”

Section: Introductionmentioning

confidence: 99%

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History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine

et al. 2014

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Childhood exposure to severe or chronic trauma is an important risk factor for the later development of adult mental health problems, such as substance abuse. Even in nonclinical samples of healthy adults, persons with a history of significant childhood adversity seem to experience greater psychological distress than those without this history. Evidence from rodent studies suggests that early life stress may impair dopamine function in ways that increase risks for drug abuse. However, the degree to which these findings translate to other species remains unclear. This study was conducted to examine associations between childhood adversity and dopamine and subjective responses to amphetamine in humans. Following intake assessment, 28 healthy male and female adults, ages 18–29 years, underwent two consecutive 90-minute positron emission tomography (PET) studies with high specific activity [11C]raclopride. The first scan was preceded by intravenous saline; the second by amphetamine (AMPH 0.3 mg/kg). Consistent with prior literature, findings showed positive associations between childhood trauma and current levels of perceived stress. Moreover, greater number of traumatic events and higher levels of perceived stress were each associated with higher ventral striatal dopamine responses to AMPH. Findings of mediation analyses further showed that a portion of the relationship between childhood trauma and dopamine release may be mediated by perceived stress. Overall, results are consistent with preclinical findings suggesting that early trauma may lead to enhanced sensitivity to psychostimulants and that this mechanism may underlie increased vulnerability for drug abuse.

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Section: Discussionmentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine

et al. 2014

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“…Behavioral or neurochemical measures taken in adulthood could overlook transient effects that might have resolved by adulthood in this ELS model. Importantly, the transient nature of ELS effects reported here and elsewhere [9] speaks to the careful nature by which animal models should be translated to clinical relevance, since animal models could lack important mediating effects of human experience that might lead to enduring dysfunction. Taken together, we report here that neonatal ELS alters later social interaction and PFC PVB, which is seen earlier in females than males and may occur through sexually dimorphic mechanisms.…”

Section: Discussionmentioning

confidence: 84%

Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than in males

Holland

Ganguly

Potter

et al. 2014

Neuroscience Letters

109

101

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Early life stress exposure (ELS) yields risk for psychiatric disorders that might occur though a population-specific mechanism that impacts prefrontal cortical development. Sex differences in ELS effects are largely unknown and are also essential to understand social and cognitive development. ELS can cause dysfunction within parvalbumin (PVB)-containing inhibitory interneurons in the prefrontal cortex and in several prefrontal cortex-mediated behaviors including social interaction. Social behavior deficits are often the earliest observed changes in psychiatric disorders, therefore the time-course and causation of social interaction deficits after ELS are important to determine. PVB interneuron dysfunction can disrupt social behavior, and has been correlated in males with elevated markers of oxidative stress and inflammation, such as cyclooxygenase-2 after ELS. Here, we measured the effects of maternal separation ELS on social interaction behaviors in males and females. Prefrontal cortex PVB and cyclooxygenase-2 were also measured in juveniles and adolescents using Western blots. ELS led to social interaction alterations earlier in females than males. Sexually dimorphic behavioral changes were consistent with prefrontal cortex PVB loss after ELS. PVB levels were decreased in ELS-exposed juvenile females, while males exposed to ELS do not display parvalbumin decreases until adolescence. Early behavioral and PVB changes in females did not appear to be mediated through cyclooxygenase-2, since levels were not affected in ELS females. Therefore, these data suggest that ELS affects males and females differently and with distinct developmental profiles.

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“…The MS procedure used in this study was described previously by Chocyk et al (2010, 2011a,b,b,b. Briefly, on PNDs 1–14, the dams and pups were removed from the maternity cages for 3 h each day (09:00–12:00 h).…”

Section: Methodsmentioning

confidence: 99%

“…1C. The total numbers of CV+ and BrdU+ cells in the SN and VTA were estimated using unbiased stereological methods (West et al, 1991) as described previously by Chocyk et al (2011a,b); Chocyk et al (2011a,b). Briefly, every third (juvenile and adolescent rats brain) or fourth section (adult rats brains), which was selected by systematic random sampling along the rostrocaudal axis of the SN and VTA, was chosen for analysis (10–11 sections per animal).…”

Section: Methodsmentioning

confidence: 99%

Early‐life stress increases the survival of midbrain neurons during postnatal development and enhances reward‐related and anxiolytic‐like behaviors in a sex‐dependent fashion

Chocyk

Majcher-Maślanka

Przyborowska

et al. 2015

Intl J of Devlp Neuroscience

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Clinical studies have suggested that early-life stress (ELS) increases the risk of psychopathologies that are strongly associated with dysfunction of dopaminergic neurotransmission. Thus, ELS may interfere with the development and maturation of the dopaminergic system; however, the mechanisms involved in such interference are poorly understood. In the present study, we investigated the effect of ELS on the survival of specific populations of neurons in the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA) during postnatal development. First, we injected bromodeoxyuridine (BrdU) into pregnant rat dams on embryonic days 12, 13 and 14 to permanently label midbrain neurons. Then, after birth, the dams and litters were subjected to a maternal separation (MS) procedure to model ELS conditions. The number of BrdU+ neurons and the total number of neurons (cresyl violet+, CV+) were estimated in both male and female juvenile, adolescent, and adult rats. Moreover, sucrose preference and anxiety-like behaviors were studied during adulthood. We found that MS permanently increased the number of BrdU+ and CV+ neurons in the VTA of males. In the SNc, a temporary increase in the number of BrdU+ neurons was observed in juvenile MS males; however, only adult MS males displayed an increase in the number of CV+ neurons. Immunofluorescence analysis implied that MS affected the fate of non-dopaminergic neurons. MS males displayed anxiolytic-like behavior and an increase in sucrose preference. These results suggest that ELS induces distinct dysregulation in the midbrain circuitry of males, which may lead to sex-specific psychopathology of the reward system.

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The impact of maternal separation on the number of tyrosine hydroxylase-expressing midbrain neurons during different stages of ontogenesis

Cited by 43 publications

References 102 publications

History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine

History of childhood adversity is positively associated with ventral striatal dopamine responses to amphetamine

Early life stress disrupts social behavior and prefrontal cortex parvalbumin interneurons at an earlier time-point in females than in males

Early‐life stress increases the survival of midbrain neurons during postnatal development and enhances reward‐related and anxiolytic‐like behaviors in a sex‐dependent fashion

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