Sensitivity of the prefrontal GABAergic system to chronic stress in male and female mice: Relevance for sex differences in stress-related disorders

Shepard, Ryan; Page, Carey P.; Coutellier, Laurence

doi:10.1016/j.neuroscience.2016.06.038

Cited by 92 publications

(121 citation statements)

References 57 publications

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“…For instance, the GABAergic pathway in corticolimbic structures seems to be affected in a sex‐specific way in response to chronic stress. Parvalbumin mRNA levels in the PFC are upregulated in females, but are unchanged in males . Other genes related to the GABAergic pathway such as Gad67 , Gad65 , and somatostatin ( Sst ) in the BLA are also strongly influenced by the interaction of stress exposure and sex .…”

Section: Chronic Stressmentioning

confidence: 99%

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Sex differences: Transcriptional signatures of stress exposure in male and female brains

Brivio

López

Chen

2020

Genes Brain and Behavior

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More than two‐thirds of patients suffering from stress‐related disorders are women but over two‐thirds of suicide completers are men. These are just some examples of the many sex differences in the prevalence and manifestations of stress‐related disorders, such as major depressive disorder, post‐traumatic stress disorder, and anxiety disorders, which have been extensively documented in clinical research. Nonetheless, the molecular origins of this sex dimorphism are still quite obscure. In response to this lack of knowledge, the NIH recently advocated implementing sex as biological variable in the design of preclinical studies across disciplines. As a result, a newly emerging field within psychiatry is trying to elucidate the molecular causes underlying the clinically described sex dimorphism. Several studies in rodents and humans have already identified many stress‐related genes that are regulated by acute and chronic stress in a sex‐specific fashion. Furthermore, current transcriptomic studies have shown that pathways and networks in male and female individuals are not equally affected by stress exposure. In this review, we give an overview of transcriptional studies designed to understand how sex influences stress‐specific transcriptomic changes in rodent models, as well as human psychiatric patients, highlighting the use of different methodological techniques. Understanding which mechanisms are more affected in males, and which in females, may lead to the identification of sex‐specific mechanisms, their selective contribution to stress susceptibility, and their role in the development of stress‐related psychiatric disorders.

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Section: Chronic Stressmentioning

confidence: 99%

“…Parvalbumin mRNA levels in the PFC are upregulated in females, but are unchanged in males. 141,142 Other genes related to the GABAergic pathway such as Gad67, Gad65, and somatostatin (Sst)…”

Section: Targeted Studiesmentioning

confidence: 99%

Sex differences: Transcriptional signatures of stress exposure in male and female brains

Brivio

López

Chen

2020

Genes Brain and Behavior

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“…For instance, social isolation causes a 40% reduction in GABA transporter 1 immunolabeling in the PFC compared to socially housed littermate rats (37). A recent analysis of parvalbumin transcript levels and number of PV-positive cells in PFC following exposure to a chronic unpredictable mild stress paradigm revealed somewhat conflicting results (38). This is intriguing, and one possible explanation could be the sustained hypoactivity of SST interneurons.…”

Section: Gaba Deficits Pfc and Stress: Insights From Animal Modelsmentioning

confidence: 99%

Prefrontal cortex GABAergic deficits and circuit dysfunction in the pathophysiology and treatment of chronic stress and depression

Ghosal

Hare

Duman

2017

Current Opinion in Behavioral Sciences

144

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Psychiatric diseases, notably major depression, are associated with imbalance of excitatory and inhibitory neurotransmission within the prefrontal cortex (PFC) and related limbic brain circuitry. In many cases these illnesses are precipitated or exacerbated by chronic stress, which also alters excitatory and inhibitory neurotransmitter systems. Notably, exposure to repeated uncontrollable stress causes persistent changes in the synaptic integrity and function of the principal glutamatergic excitatory neurons in the PFC, characterized by neuronal atrophy and loss of synaptic connections. This can lead to dysfunction of the PFC circuitry that is necessary for execution of adaptive behavioral responses. In addition, an emerging literature shows that chronic stress also causes extensive alteration of GABAergic inhibitory circuits in the PFC, leading to the hypothesis that inhibitory neurotransmitter deficits contribute to changes in PFC neuronal excitability and cognitive impairments. Here we review evidence in rodents and human, which point to the mechanisms underlying stress-induced alterations of GABA transmission in the PFC, and its relevance to circuit dysfunction in mood and stress related disorders. These findings suggest that alterations of GABA interneurons and inhibitory neurotransmission play a causal role in the development of stress-related neurobiological illness, and could identify a new line of GABA related therapeutic targets.

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“…Because we measured multiple behavioral parameters on each individual duckling, we condensed these non‐independent measures from all trials into two values for each individual using a z ‐score analysis, as described in Guilloux, Seney, Edgar, and Sibille () and Labots, Laarakker, Schetters, Arndt, and van Lith (). This statistical technique has been used in studies to measure emotionality in mice from multiple trials (e.g., Mendez‐David et al., ; Piantadosi et al., ; Shepard et al., ; Zemdegs et al., ). It is an improved way to quantify behavior when using multiple trials because it reduces variance and increases reliability of behavioral measures, compared to using the raw behavioral data (Guilloux et al., ).…”

Section: Methodsmentioning

confidence: 99%

Incubation temperature influences the behavioral traits of a young precocial bird

et al. 2018

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The environment in which animals develop can have important consequences for their phenotype. In reptiles, incubation temperature is a critical aspect of the early developmental environment. Incubation temperature influences morphology, physiology, and behavior of non-avian reptiles, however, little is known about how incubation temperature influences offspring phenotype and behaviors important to avian survival. To investigate whether incubation temperature influences avian behaviors, we collected wood duck (Aix sponsa) eggs from the field and incubated them at three naturally occurring incubation temperatures (35.0, 35.8, and 37.0°C). We conducted multiple repeated behavioral trials on individual ducklings between 5 and 15 days post-hatch to assess activity, exploratory, and boldness behaviors, classified along a proactive-reactive continuum. We measured growth rates and circulating levels of baseline and stress-induced corticosterone levels to investigate possible physiological correlates of behavior. Ducklings incubated at the lowest temperature displayed more proactive behaviors than those incubated at the two higher temperatures. We also found that younger ducklings exhibited more proactive behavior than older ducklings and males exhibited more proactive behavior than females. Further, duckling behaviors were repeatable across time and contexts, indicative of a proactive-reactive continuum of behavioral tendencies. However, neither corticosterone levels nor growth rates were related to behavior. This provides some of the first evidence that incubation temperature, a critical parental effect, influences avian offspring behaviors that may be important for survival. Our results identify incubation temperature as a mechanism that contributes to the development of behavioral traits and, in part, explains how multiple behavioral types may be maintained within populations.

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Sensitivity of the prefrontal GABAergic system to chronic stress in male and female mice: Relevance for sex differences in stress-related disorders

Cited by 92 publications

References 57 publications

Sex differences: Transcriptional signatures of stress exposure in male and female brains

Sex differences: Transcriptional signatures of stress exposure in male and female brains

Prefrontal cortex GABAergic deficits and circuit dysfunction in the pathophysiology and treatment of chronic stress and depression

Incubation temperature influences the behavioral traits of a young precocial bird

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