Age-dependent shift in spontaneous excitation-inhibition balance of infralimbic prefrontal layer II/III neurons is accelerated by early life stress, independent of forebrain mineralocorticoid receptor expression

Karst, H.; Sarabdjitsingh, R. Angela; Weerd, Nelleke van der; Feenstra, Eline; Damsteegt, Ruth; Joëls, Marian

doi:10.1016/j.neuropharm.2020.108294

Cited by 19 publications

(28 citation statements)

References 80 publications

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“…The ELS-induced reduction in non-monotonic ACx cells (Fig 6H) also points to inhibitory changes, as non-monotonicity in ACx is shaped by local inhibition (Wu et al, 2006). Similarly, altered inhibitory function in prefrontal cortex, hippocampus, and amygdala arising from ELS coincides with emotional and cognitive problems (Brenhouse and Andersen, 2011; Bath et al, 2016; Castillo-Gomez et al, 2017; Murthy et al, 2019; Page and Coutellier, 2019; Karst et al, 2020; Manzano Nieves et al, 2020). ELS causes early maturation of perineuronal nets, reduction in inhibitory neurons, and changes in BDNF levels in frontal cortex and amygdala (Cameron et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Mattingly

Sunthimer

et al. 2022

Preprint

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In children, early ear infections are a risk factor for later speech perception deficits. This is likely because auditory deprivation during a developmental critical period (CP) induces long-lasting deficits in perception and ACx encoding of temporally-varying sounds. CPs also create susceptibility to early-life stress (ELS) in neural regions involved with cognition and anxiety. As CP mechanisms are shared by sensory cortices and higher neural regions, ACx and temporal encoding may also be susceptible to ELS. To examine the effects of ELS on temporal processing, we developed a model of ELS in the Mongolian gerbil, a well-established model for auditory processing. ELS induction impaired the behavioral detection of short gaps in sound, which are critical for speech perception. This was accompanied by reduced neural responses to gaps in ACx, the auditory periphery, and auditory brainstem. These ELS effects presumably degrade the fidelity of sensory representations available to higher regions, and could contribute to ELS-induced problems with cognition.

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Section: Discussionmentioning

confidence: 99%

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Mattingly

Sunthimer

et al. 2022

Preprint

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“…On postnatal day (P) 2 the litter was randomly assigned to either the control condition (standard housing) or the ELS condition. In the ELS condition a limited amount of nesting and bedding material was made available between P2 and P9 (Karst et al, 2020; Naninck et al, 2015; Rice et al, 2008). All animal experiments were performed in compliance with the guidelines for the welfare of experimental animals and were approved by the Dutch Central Committee Animal experiments (CCD), project AVD1150020184927.…”

Section: Methodsmentioning

confidence: 99%

Using SuperClomeleon to measure changes in intracellular chloride during development and after early life stress

Wierenga

Herstel

Peerboom

et al. 2022

Preprint

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Intraneuronal chloride concentrations ([Cl-]i) decrease during development resulting in a shift from depolarizing to hyperpolarizing γ-aminobutyric acid (GABA) responses via chloride-permeable GABAA receptors. This GABA shift plays a pivotal role in postnatal brain development, and can be strongly influenced by early life experience. Here, we assessed the applicability of the recently developed fluorescent SuperClomeleon (SClm) sensor to examine changes in [Cl-]i using two-photon microscopy in brain slices. We used SClm mice of both sexes to monitor the developmental decrease in neuronal chloride levels in organotypic hippocampal cultures. We could discern a clear reduction in [Cl-]i between DIV3 and DIV9 (equivalent to the second postnatal week in vivo) and a further decrease in some cells until DIV22. In addition, we assessed alterations in [Cl-]i in the medial prefrontal cortex (mPFC) of P9 male SClm mouse pups after early life stress (ELS). ELS was induced by limiting nesting material between P2 and P9. ELS induced a shift towards higher (i.e. immature) chloride levels in layer 2/3 cells in the mPFC. Although conversion from SClm fluorescence to absolute chloride concentrations proved difficult, our study underscores that the SClm sensor is a powerful tool to measure physiological changes in [Cl-]i in brain slices.

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“…ELS induced by maternal separation in rats accelerates synaptic activity in hippocampus; thus, LTP peaks in adolescence (P22–24) but not in adulthood [ 202 ], and age-dependent shift in spontaneous excitatory synaptic currents relative to inhibitory synaptic currents was significantly accelerated by ELS in mice [ 203 ]. ELS-induced changes in E/I balance are not specific for hippocampus, since neurons in the prefrontal area [ 204 ] and infralimbic prefrontal layer II/III [ 203 ] are affected as well. In sum, E/I balance is greatly affected in ELS, thereby contributing to the changes in stem and progenitor cells proliferation and differentiation.…”

Section: Neurogenesis and Cerebral Angiogenesis: Search For A Common Regulator Of Metabolic Reprogrammingmentioning

confidence: 99%

Early Life Stress and Metabolic Plasticity of Brain Cells: Impact on Neurogenesis and Angiogenesis

et al. 2021

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Early life stress (ELS) causes long-lasting changes in brain plasticity induced by the exposure to stress factors acting prenatally or in the early postnatal ontogenesis due to hyperactivation of hypothalamic-pituitary-adrenal axis and sympathetic nervous system, development of neuroinflammation, aberrant neurogenesis and angiogenesis, and significant alterations in brain metabolism that lead to neurological deficits and higher susceptibility to development of brain disorders later in the life. As a key component of complex pathogenesis, ELS-mediated changes in brain metabolism associate with development of mitochondrial dysfunction, loss of appropriate mitochondria quality control and mitochondrial dynamics, deregulation of metabolic reprogramming. These mechanisms are particularly critical for maintaining the pool and development of brain cells within neurogenic and angiogenic niches. In this review, we focus on brain mitochondria and energy metabolism related to tightly coupled neurogenic and angiogenic events in healthy and ELS-affected brain, and new opportunities to develop efficient therapeutic strategies aimed to restore brain metabolism and reduce ELS-induced impairments of brain plasticity.

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Age-dependent shift in spontaneous excitation-inhibition balance of infralimbic prefrontal layer II/III neurons is accelerated by early life stress, independent of forebrain mineralocorticoid receptor expression

Abstract: Age-dependent shift in spontaneous excitation-inhibition balance of infralimbic prefrontal layer II/III neurons is accelerated by early life stress, independent of forebrain mineralocorticoid receptor expression

Cited by 19 publications

References 80 publications

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Early-Life Stress Impairs Perception and Neural Encoding of Rapid Signals in the Auditory Pathway

Using SuperClomeleon to measure changes in intracellular chloride during development and after early life stress

Early Life Stress and Metabolic Plasticity of Brain Cells: Impact on Neurogenesis and Angiogenesis

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