Juvenile stress-induced alteration of maturation of the GABAA receptor α subunit in the rat

Jacobson‐Pick, Shlomit; Elkobi, Alina; Vander, Shelly; Rosenblum, Kobi; Richter‐Levin, Gal

doi:10.1017/s1461145708008559

Cited by 59 publications

(46 citation statements)

References 54 publications

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“…The reduction of activity/exploration in novel environments has been interpreted as reflective of anhedonic-like behavior (Fukushiro et al, 2012). The lack of anxiogenic effects of the present model contrasts with other previous reports (Avital et al, 2006;Bazak et al, 2009;Ilin and Richter-Levin, 2009;Jacobson-Pick and Richter-Levin, 2012;Jacobson-Pick et al, 2008;Tsoory et al, 2007Tsoory et al, , 2010. Although this might suggest that our procedure is of lower intensity than previous protocols, this is difficult to demonstrate and not supported by the observed reduction of body weight gain.…”

Section: Accepted M Manuscriptcontrasting

confidence: 97%

“…This contrasts with previous reports of increased anxiety (Giovanoli et al, 2013;Jacobson-Pick et al, 2008;Maslova et al, 2002aMaslova et al, , 2002bTsoory et al, 2007;Yee et al, 2011), although negative or inconsistent results have also been reported (Avital and Richter-Levin, 2005;Bourke and Neigh, 2011;Jacobson-Pick and Richter-Levin, 2010;McCormick et al, 2007;Peleg-Raibstein and Feldon, 2011;Pohl et al, 2007;Toledo-Rodríguez and Sandi, 2007). This is likely related to a differential susceptibility to stress among the different strains of rats and mice used (e.g., Maslova et al, 2002aMaslova et al, , 2002b.…”

Section: Accepted M Manuscriptcontrasting

confidence: 87%

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Behavioral and neuroendocrine consequences of juvenile stress combined with adult immobilization in male rats

Fuentes

Carrasco

Armario

et al. 2014

Hormones and Behavior

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Exposure to stress during childhood and adolescence increases vulnerability to developing several psychopathologies in adulthood and alters the activity of the hypothalamic-pituitaryadrenal (HPA) axis, the prototypical stress system. Rodent models of juvenile stress appear to support this hypothesis because juvenile stress can result in reduced activity/exploration and enhanced anxiety, although results are not always consistent. Moreover, an in-depth characterization of changes in the HPA axis is lacking. In the present study, the long-lasting effects of juvenile stress on adult behavior and HPA function were evaluated in male rats. The juvenile stress consisted of a combination of stressors (cat odor, forced swim and footshock) during postnatal days 23-28. Juvenile stress reduced the maximum amplitude of the adrenocorticotropic hormone (ACTH) levels (reduced peak at lights off), without affecting the circadian corticosterone rhythm, but other aspects of the HPA function (negative glucocorticoid feedback, responsiveness to further stressors and brain gene expression of corticotrophin-releasing hormone and corticosteroid receptors) remained unaltered. The behavioral effects of juvenile stress itself at adulthood were modest (decreased activity in the circular corridor) with no evidence of enhanced anxiety. Imposition of an acute severe stressor (immobilization on boards, IMO) did not increase anxiety in control animals, as evaluated one week later in the elevated-plus maze (EPM), but it potentiated the acoustic startle response (ASR). However, acute IMO did enhance anxiety in the EPM, in juvenile stressed rats, thereby suggesting that juvenile stress sensitizes rats to the effects of additional stressors.

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Section: Accepted M Manuscriptcontrasting

confidence: 97%

Section: Accepted M Manuscriptcontrasting

confidence: 87%

Behavioral and neuroendocrine consequences of juvenile stress combined with adult immobilization in male rats

Fuentes

Carrasco

Armario

et al. 2014

Hormones and Behavior

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“…Given increased levels of GABA Aα2 mRNA in the amygdala are found in stressed animals (38), the reductions in GABA receptor subunits induced by the Lactobacillus suggest that this bacteria could have promoted an adaptive advantage over broth-fed animals in terms of interaction with stressful situations. The amygdala is also necessary for conditioning of a relatively simple stimulus or cue (conditioned stimulus) and the context in which the unconditioned stimulus is delivered (24,25).…”

Section: Discussionmentioning

confidence: 99%

“…L. rhamnosus (JB-1) administration also affected the transcripts of GABA A receptor subunits in the hippocampus. Although differences in the expression of the transcript for GABA Aα2 and GABA Aα1 have been found in the hippocampus of rats subjected to different learning tasks, these changes are not consistent (38,42). Nevertheless, it has been shown that GABA A receptors bearing the GABA Aα2 subunit mediate the anxiolytic effects of benzodiazepines, whereas GABA A receptors that have the α1 subunit mediate the sedative and amnesic effects of benzodiazepines (12).…”

Section: Discussionmentioning

confidence: 99%

Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve

Bravo¹,

Forsythe

Chew

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

3,127

2,512

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There is increasing, but largely indirect, evidence pointing to an effect of commensal gut microbiota on the central nervous system (CNS). However, it is unknown whether lactic acid bacteria such as Lactobacillus rhamnosus could have a direct effect on neurotransmitter receptors in the CNS in normal, healthy animals. GABA is the main CNS inhibitory neurotransmitter and is significantly involved in regulating many physiological and psychological processes. Alterations in central GABA receptor expression are implicated in the pathogenesis of anxiety and depression, which are highly comorbid with functional bowel disorders. In this work, we show that chronic treatment with L. rhamnosus (JB-1) induced region-dependent alterations in GABA B1b mRNA in the brain with increases in cortical regions (cingulate and prelimbic) and concomitant reductions in expression in the hippocampus, amygdala, and locus coeruleus, in comparison with control-fed mice. In addition, L. rhamnosus (JB-1) reduced GABA Aα2 mRNA expression in the prefrontal cortex and amygdala, but increased GABA Aα2 in the hippocampus. Importantly, L. rhamnosus (JB-1) reduced stress-induced corticosterone and anxiety-and depression-related behavior. Moreover, the neurochemical and behavioral effects were not found in vagotomized mice, identifying the vagus as a major modulatory constitutive communication pathway between the bacteria exposed to the gut and the brain. Together, these findings highlight the important role of bacteria in the bidirectional communication of the gut-brain axis and suggest that certain organisms may prove to be useful therapeutic adjuncts in stressrelated disorders such as anxiety and depression.brain-gut axis | irritable bowel syndrome | probiotic | fear conditioning | cognition T here is increasing evidence suggesting an interaction between the intestinal microbiota, the gut, and the central nervous system (CNS) in what is recognized as the microbiome-gut-brain axis (1-4). Studies in rodents have implicated dysregulation of this axis in functional bowel disorders, including irritable bowel syndrome. Indeed, visceral perception in rodents can be affected by alterations in gut microbiota (5). Moreover, it has been shown that the absence and/or modification of the gut microflora in mice affects the hypothalamic-pituitary-adrenal (HPA) axis response to stress (6, 7) and anxiety behavior (8, 9), which is important given the high comorbidity between functional gastrointestinal disorders and stress-related psychiatric disorders, such as anxiety and depression (10). In addition, pathogenic bacteria in rodents can induce anxiety-like behaviors, which are mediated via vagal afferents (9, 11).GABA is the main inhibitory neurotransmitter of the CNS, the effects of which are mediated through two major classes of receptors-the ionotropic GABA A receptors, which exist as a number of subtypes formed by the coassembly of different subunits (α, β, and γ subunits; ref. 12), and the GABA B receptors, which are G protein coupled and consist of a heterodi...

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“…While most ELS rodent models focus on the perinatal to pre-weaning periods and involve some form of maternal deprivation or separation (for a review, see [25]), we have focused in recent years on an alternative period in the rat ontogeny, ‘juvenility’ (∼28 days), the earlier phase of the adolescent/post-weaning to pre-pubertal period [26,27,30,31,38,44,45,46,49,51,59] (for a summary of the main findings, see tables 1 and 2). …”

Section: Post-weaning To Pre-pubertal (Juvenile) Stress Modelmentioning

confidence: 99%

Post-Weaning to Pre-Pubertal (‘Juvenile’) Stress: A Model of Induced Predisposition to Stress-Related Disorders

et al. 2012

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Human studies suggest that childhood trauma predisposes individuals to develop stress-related disorders such as depression and post-traumatic stress disorder (PTSD). Recent years have witnessed growing interest in effectively modeling in animals the long-term effects of childhood emotional trauma on stress responses in adulthood. Most studies concerned with the impact of early-life stress on subsequent stress responses in adulthood in rodents have focused on the post-natal pre-weaning period. However, psychiatric studies often refer to human childhood rather than infancy when investigating the patients’ traumatic history of stress-related psychopathologies. In accordance with that, we have examined the consequences of stress exposure at a later early-life period, the post-weaning, pre-puberty (juvenile) period, which holds greater resemblance to human childhood. This review summarizes a series of studies examining the impact of exposure of rats to stressors during ‘juvenility’ (‘juvenile stress’) on the ability of these animals to cope with stress later in life. Exposure to relatively brief but significant stress experience during juvenility was found to impair the ability of animals to cope with stressful challenges in adulthood. These behavioral manifestations were associated with lasting alterations in limbic system brain regions of neuromodulatory pathways, such as alterations in the expression of cell adhesion molecules, GABAergic system functioning and alterations in levels of circulating corticosterone. Importantly, these studies have also demonstrated considerable individual and sex differences, which call for the development of adequate analysis approaches. The juvenile stress model combined with characterization of individual profiles is presented as a useful model to study in rodents different facets of stress-related disorders and neural mechanisms of vulnerability and resilience to stress.

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Juvenile stress-induced alteration of maturation of the GABAA receptor α subunit in the rat

Cited by 59 publications

References 54 publications

Behavioral and neuroendocrine consequences of juvenile stress combined with adult immobilization in male rats

Behavioral and neuroendocrine consequences of juvenile stress combined with adult immobilization in male rats

Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve

Post-Weaning to Pre-Pubertal (‘Juvenile’) Stress: A Model of Induced Predisposition to Stress-Related Disorders

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