Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats

Koss, Wendy A.; Lloyd, Madeline M.; Sadowski, Renee N.; Wise, Leslie; Juraska, Janice M.

doi:10.1002/dev.21290

Cited by 84 publications

(78 citation statements)

References 40 publications

(68 reference statements)

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“…Here, we examine the trajectory of the neuronal losses took place between P35 and P45. Ovariectomy before puberty at P20 prevented this neuronal loss in females compared to intact females by adulthood (Koss et al, 2015), suggesting that ovarian hormones may play a role in the pruning of neurons. In the present study, neuronal losses coincided with pubertal onset provides more support for a role of ovarian hormones at puberty in the development of the PFC in adolescent females.…”

Section: Discussionmentioning

confidence: 96%

“…In the rat mPFC, the number of neurons decreases between adolescence and adulthood with neuronal loss being considerably greater in females (Markham et al, 2007). There is further evidence that in females, the actions of hormones secreted after puberty lead to this decrease in mPFC neuron number, as ovariectomy before puberty prevents this loss when neuron number is assessed in adulthood (Koss et al, 2015). This is similar to findings in the primary visual cortex where ovarian hormones after puberty were found to play a role in neuronal pruning (Nuñez et al, 2002).…”

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confidence: 99%

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The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats

Willing¹,

Juraska²

2015

Neuroscience

144

111

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Adolescence is a critical period for brain maturation characterized by the reorganization of interacting neural networks. In particular the prefrontal cortex, a region involved in executive function, undergoes synaptic and neuronal pruning during this time in both humans and rats. Our laboratory has previously shown that rats lose neurons in the medial prefrontal cortex (mPFC) and there is an increase in white matter under the frontal cortex between adolescence and adulthood. Female rats lose more neurons during this period, and ovarian hormones may play a role as ovariectomy before adolescence prevents neuronal loss. However, little is known regarding the timing of neuroanatomical changes that occur between early adolescence and adulthood. In the present study, we quantified the number of neurons and glia in the male and female mPFC at multiple time points from preadolescence through adulthood (postnatal days 25, 35, 45, 60 and 90). Females, but not males, lost a significant number of neurons in the mPFC between days 35 and 45, coinciding with the onset of puberty. Counts of GABA immunoreactive cell bodies indicated that the neurons lost were not primarily GABAergic. These results suggest that in females, pubertal hormones may exert temporally specific changes in PFC anatomy. As expected, both males and females gained white matter under the prefrontal cortex throughout adolescence, though these gains in females were diminished after day 35, but not in males. The differences in cell loss in males and females may lead to differential vulnerability to external influences and dysfunctions of the prefrontal cortex that manifest in adolescence.

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Section: Discussionmentioning

confidence: 96%

mentioning

confidence: 99%

The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats

Willing¹,

Juraska²

2015

Neuroscience

144

111

View full text Add to dashboard Cite

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“…For example, there is a loss of volume during adolescence, which is at least partially attributable to a loss of neurons, which is more significant in females [41]. Moreover, in adult rats, medial frontal pyramidal neurons are more complex, and the synaptic density is higher in males [33].…”

Section: Discussionmentioning

confidence: 99%

Neonatal Stress Has a Long-Lasting Sex-Dependent Effect on Anxiety-Like Behavior and Neuronal Morphology in the Prefrontal Cortex and Hippocampus

et al. 2018

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The long-lasting effects of early stress on brain development have been well studied. Recent evidence indicates that males and females respond differently to the same stressor. We examined the chronic effects of daily maternal separation (MS) on behavior and cerebral morphology in both male and female rats. Cognitive and anxiety-like behaviors were evaluated, and neuroplastic changes in 2 subregions of the prefrontal cortex (dorsal agranular insular cortex [AID] and cingulate cortex [Cg3]) and hippocampus (CA1 and dentate gyrus) were measured in adult male and female rats. The animals were subjected to MS on postnatal day (P) 3–14 for 3 h per day. Cognitive and emotional behaviors were assessed in the object/context mismatch task, elevated plus maze, and locomotor activity test in early adulthood (P87–P95). Anatomical assessments were performed in the prefrontal cortex (i.e., cortical thickness and spine density) and hippocampus (i.e., spine density). Sex-dependent effects were observed. MS increased anxiety-related behavior only in males, whereas locomotor activity was higher in females, with no effects on cognition. MS decreased spine density in the AID and increased spine density in the CA1 area in males. Females exhibited an increase in spine density in the Cg3. Our findings confirm previous work that found that MS causes long-term behavioral and anatomical effects, and these effects were dependent on sex and the duration of MS stress.

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“…This decline in humans and rats coincides with the average onset of puberty, suggesting a hormonal role in cortical restructuring. To support this hypothesis, Koss et al (2015)) found that pre-pubertal gonadectomy did not have an effect in males, but prevented the neuron and glial loss in the mPFC in female rats, suggesting that ovarian hormones are involved in the loss of cortical neurons during adolescence. Given that gonadal hormones appear to be involved in the cortical restructuring that occurs during adolescence, it is plausible that endocrine disruptors, such as BPA, could alter normal development.…”

Section: Introductionmentioning

confidence: 99%

Long-term effects of adolescent exposure to bisphenol A on neuron and glia number in the rat prefrontal cortex: Differences between the sexes and cell type

et al. 2016

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Bisphenol A (BPA), an endocrine disruptor used in a variety of consumer products, has been found to alter the number of neurons in multiple brain areas in rats following exposure in perinatal development. Both the number of neurons and glia also change in the medial prefrontal cortex (mPFC) during adolescence, and this process is known to be influenced by gonadal hormones which could be altered by BPA. In the current study, we examined Long-Evans male and female rats that were administered BPA (0, 4, 40, or 400 µg/kg/day) during adolescent development (postnatal days 27–46). In adulthood (postnatal day 150), the number of neurons and glia in the mPFC were stereologically assessed in methylene blue/azure II stained sections. There were no changes in the number of neurons, but there was a significant dose by sex interaction in number of glia in the mPFC. Pairwise comparisons between controls and each dose showed a significant increase in the number of glia between 0 and 40 µg/kg/day in females, and a significant decrease in the number of glia between 0 and 4 µg/kg/day in males. In order to determine the type of glial cells that were changing in these groups in response to adolescent BPA administration, adjacent sections were labelled with S100β (astrocytes) and IBA-1 (microglia) in the mPFC of the groups that differed. The number of microglia was significantly higher in females exposed to 40 µg/kg/day than controls and lower in males exposed to 4 µg/kg/day than controls. There were no significant effects of adolescent exposure to BPA on the number of astrocytes in male or females. Thus, adolescent exposure to BPA produced long-term alterations in the number of microglia in the mPFC of rats, the functional implications of which need to be explored.

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Gonadectomy before puberty increases the number of neurons and glia in the medial prefrontal cortex of female, but not male, rats

Cited by 84 publications

References 40 publications

The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats

The timing of neuronal loss across adolescence in the medial prefrontal cortex of male and female rats

Neonatal Stress Has a Long-Lasting Sex-Dependent Effect on Anxiety-Like Behavior and Neuronal Morphology in the Prefrontal Cortex and Hippocampus

Long-term effects of adolescent exposure to bisphenol A on neuron and glia number in the rat prefrontal cortex: Differences between the sexes and cell type

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