Imbalance of immunohistochemically characterized interneuron populations in the adolescent and adult rodent medial prefrontal cortex after repeated exposure to neonatal separation stress

Helmeke, Carina; Ovtscharoff, Wladimir; Poeggel, Gerd; Braun, Katharina

doi:10.1016/j.neuroscience.2007.12.023

Cited by 71 publications

(66 citation statements)

References 81 publications

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“…CRF-containing cell bodies are present in most layers of the rat PFC and at least some of these cell bodies are GABAergic interneurons (Helmeke et al, 2008;Mohila, 2004). However, whether interneurons comprise the entire population of CRF cell bodies within the PFC is unclear.…”

Section: Discussionmentioning

confidence: 99%

Working Memory Impairing Actions of Corticotropin-Releasing Factor (CRF) Neurotransmission in the Prefrontal Cortex

Hupalo

Berridge

2016

Neuropsychopharmacol

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The prefrontal cortex (PFC) regulates cognitive processes critical for goal-directed behavior. PFC cognitive dysfunction is implicated in multiple psychopathologies, including attention deficit hyperactivity disorder (ADHD). Although it has long been known that corticotropin-releasing factor (CRF) and CRF receptors are prominent in the PFC, the cognitive effects of CRF action within the PFC are poorly understood. The current studies examined whether CRF receptor activation in the PFC modulates cognitive function in rats as measured in a delayed response task of spatial working memory. CRF dose-dependently impaired working memory performance when administered either intracerebroventricularly (ICV) or directly into the PFC. The working memory actions of CRF in the PFC were topographically organized, with impairment observed only following CRF infusions into the caudal dorsomedial PFC (dmPFC). Additional studies examined whether endogenous CRF modulates working memory. Both ICV and intra-dmPFC administration of the nonselective CRF antagonist, D-Phe-CRF, dose-dependently improved working memory performance. To better assess the translational potential of CRF antagonists, we examined the cognitive effects of systemic administration of the CRF1 receptor selective antagonist, NBI 35965. Similar procognitive actions were observed in these studies. These results are the first to demonstrate that CRF acts in the PFC to regulate PFC-dependent cognition. Importantly, the ability of CRF antagonists to improve working memory is identical to that seen with all approved treatments for ADHD. These observations suggest that CRF antagonists may represent a novel approach for the treatment of ADHD and other disorders associated with dysregulated prefrontal cognitive function.

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Section: Discussionmentioning

confidence: 99%

Working Memory Impairing Actions of Corticotropin-Releasing Factor (CRF) Neurotransmission in the Prefrontal Cortex

Hupalo

Berridge

2016

Neuropsychopharmacol

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“…The PFC is a relatively late-maturing region (Alexander and Goldman, 1978) and subserves all higher-order cognitive and emotional functions. Notably, most consequences of MS in the PFC typically manifest later in life (Chocyk, Dudys, Przyborowska, Mackowiak, & Wedzony, 2010; Helmeke, Ovtscharoff, Poeggel, & Braun, 2008; Stevenson, Marsden, & Mason, 2008) probably due to its late and protracted development. The late maturation of the PFC is also a purported factor driving the “two-hit” hypothesis of psychiatric illness; a distinct developmental insult can prime an individual for a later event that ultimately leads to onset of the full clinical syndrome (Bayer, Falkai, & Maier, 1999; Deslauriers, Racine, Sarret, & Grignon, 2014).…”

mentioning

confidence: 99%

Adolescent food restriction in rats alters prefrontal cortex microglia in an experience-dependent manner

Ganguly

Thompson

Gildawie

et al. 2018

Stress

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Microglia are resident immune cells of the brain that can regulate neural communication and excitability. Any environmental influence on microglial activity has the potential to alter subsequent neural physiology and behavior. Within the prefrontal cortex, several types of stressors have been shown to increase microglial expression of activation markers such as ionized calcium-binding adapter molecule-1 (Iba-1), which suggests altered microglial activity. Recent reports in rodents suggest that exposure to forms of early-life stress such as maternal separation can alter microglial responsivity to subsequent challenges. Several learning paradigms used in rodents require food restriction to provoke motivational states that facilitate approach behaviors. Here, we tested whether food restriction (increasing from 13 g/day-23 g/day in males and 10 g/day-20 g/day in females, which reduced body weight to 72-84% free-fed weight) in adolescent rats is a sufficient challenge to affect microglial Iba-1 expression, and whether previous exposure to postnatal maternal separation influenced microglial outcomes. We measured prefrontal cortex Iba-1 expression and microglial morphology after 20 days of ad libitum or restricted food availability in males and females with or without exposure to maternal separation. Food-restricted animals displayed higher levels of Iba-1 in the prefrontal cortex, with hyper-ramified microglial morphology in maternally separated males and control females, compared to those that were free-fed. Together, our data provide evidence that food restriction paradigms may have unintended effects in some behavioral protocols.

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“…Compared to H, MS reduces the expression of glucocorticoid receptors in mPFC (Ladd et al, 2004), suggesting a possible mechanism by which negative feedback of HPA axis function is impaired in these animals. Furthermore, MS may alter dopamine and GABA transmission in mPFC (Matthews et al, 2001;Helmeke et al, 2008). Compared to undisturbed controls, basal mPFC do-pamine levels are increased and stress-induced dopamine release in mPFC is attenuated with maternal deprivation (Jezierski et al, 2007).…”

mentioning

confidence: 99%

Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex

et al. 2008

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Abstract-Neonatal maternal separation (MS) in the rat increases the vulnerability to stressors later in life. In contrast, brief handling (H) in early life confers resilience to stressors in adulthood. Early life programming of stress reactivity may involve the medial prefrontal cortex (mPFC), a region which modulates various stress responses. Moreover, hemispheric specialization in mPFC may mediate adaptive coping responses to stress. In the present study, neuronal activity was examined simultaneously in left and right mPFC in adult rats previously subjected to MS, H or animal facility rearing (AFR). In vivo electrophysiology, under isoflurane anesthesia, was used to conduct acute recordings of unit and local field potential (LFP) activity in response to systemic administration of N-methyl-␤-carboline-3-carboxamide (FG-7142), a benzodiazepine receptor partial inverse agonist which mimics various stress responses. MS decreased basal unit activity selectively in right mPFC. Basal LFP activity was reduced with MS in left and right mPFC, compared to AFR and H, respectively. Hemispheric synchronization of basal LFP activity was also attenuated by MS at lower frequencies. FG-7142 elicited lateralized effects on mPFC activity with different early rearing conditions. Activity in left mPFC was greater with AFR and MS (AFR>MS), whereas activity was predominantly greater with H in right mPFC. Finally, compared to AFR, MS reduced and H enhanced hemispheric synchronization of LFP activity with FG-7142 treatment in a dose-dependent manner.These results indicate that functionally-relevant alterations in mPFC GABA transmission are programmed by the early rearing environment in a hemisphere-dependent manner. These findings may model the hemispheric specialization of mPFC function thought to mediate adaptive coping responses to stressors. They also suggest the possibility that early environmental programming of hemispheric functional coupling in mPFC is involved in conferring vulnerability or resilience to stressors later in life.

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Imbalance of immunohistochemically characterized interneuron populations in the adolescent and adult rodent medial prefrontal cortex after repeated exposure to neonatal separation stress

Cited by 71 publications

References 81 publications

Working Memory Impairing Actions of Corticotropin-Releasing Factor (CRF) Neurotransmission in the Prefrontal Cortex

Working Memory Impairing Actions of Corticotropin-Releasing Factor (CRF) Neurotransmission in the Prefrontal Cortex

Adolescent food restriction in rats alters prefrontal cortex microglia in an experience-dependent manner

Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex

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