Does maternal separation accelerate maturation of perineuronal nets and parvalbumin-containing inhibitory interneurons in male and female rats?

Richardson, Rick; Bowers, Jeremy W.; Callaghan, Brid; Baker, Kathryn

doi:10.1016/j.dcn.2020.100905

Cited by 11 publications

(15 citation statements)

References 57 publications

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“…Interestingly, the research overviewed here suggests males and females may be differentially susceptible to ELA-induced PV pathology, particularly following MS. Specifically, in those studies examining both sexes, female PV outcomes were either comparable to those seen in males (a decrease or no change compared to controls; Leussis et al, 2012;Guadagno et al, 2020;Soares et al, 2020;Gildawie et al, 2021;Richardson et al, 2021), or females showed a lack of PV decrease while males showed a marked decrease in PV expression following ELA (do Prado et al, 2016;Grassi-Oliveira et al, 2016;Gildawie et al, 2020). Even more intriguing, was that Holland et al (2014) revealed an age-dependent decrease in the PFC after MS, with females showing earlier decreases in PV than males.…”

Section: Discussionmentioning

confidence: 99%

“…There is also evidence suggesting that ELA, specifically MS, may have a delayed impact on PV cell density. Brains that were collected immediately (or within a few days) after ELA experience generally had no significant differences in PV levels compared to control-rearing (Giachino et al, 2007 ; Brenhouse and Andersen, 2011 ; Soares et al, 2020 ; Richardson et al, 2021 ), while brains collected later in life (in adolescence and/or P40 and older) generally had decreased PV levels (Leussis et al, 2012 ; Wieck et al, 2013 ; Ganguly et al, 2015 ; Lukkes et al, 2017 , 2018 ; Kim et al, 2020 ; Aksic et al, 2021 ). Since PV cells have been found to increase significantly in number from juvenility to adolescence in brain regions such as the PFC (Caballero et al, 2014 ; Wu et al, 2014 ), it is possible that ELA may inhibit the maturational time course of PV cells.…”

Section: Introductionmentioning

confidence: 98%

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Sex Differences in Affective Dysfunction and Alterations in Parvalbumin in Rodent Models of Early Life Adversity

Ellis

Ganguly

2021

Front. Behav. Neurosci.

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The early life environment markedly influences brain and behavioral development, with adverse experiences associated with increased risk of anxiety and depressive phenotypes, particularly in females. Indeed, early life adversity (ELA) in humans (i.e., caregiver deprivation, maltreatment) and rodents (i.e., maternal separation, resource scarcity) is associated with sex-specific emergence of anxious and depressive behaviors. Although these disorders show clear sex differences in humans, little attention has been paid toward evaluating sex as a biological variable in models of affective dysfunction; however, recent rodent work suggests sex-specific effects. Two widely used rodent models of ELA approximate caregiver deprivation (i.e., maternal separation) and resource scarcity (i.e., limited bedding). While these approaches model aspects of ELA experienced in humans, they span different portions of the pre-weaning developmental period and may therefore differentially contribute to underlying mechanistic risk. This is borne out in the literature, where evidence suggests differences in trajectories of behavior depending on the type of ELA and/or sex; however, the neural underpinning of these differences is not well understood. Because anxiety and depression are thought to involve dysregulation in the balance of excitatory and inhibitory signaling in ELA-vulnerable brain regions (e.g., prefrontal cortex, amygdala, hippocampus), outcomes are likely driven by alterations in local and/or circuit-specific inhibitory activity. The most abundant GABAergic subtypes in the brain, accounting for approximately 40% of inhibitory neurons, contain the calcium-binding protein Parvalbumin (PV). As PV-expressing neurons have perisomatic and proximal dendritic targets on pyramidal neurons, they are well-positioned to regulate excitatory/inhibitory balance. Recent evidence suggests that PV outcomes following ELA are sex, age, and region-specific and may be influenced by the type and timing of ELA. Here, we suggest the possibility of a combined role of PV and sex hormones driving differences in behavioral outcomes associated with affective dysfunction following ELA. This review evaluates the literature across models of ELA to characterize neural (PV) and behavioral (anxiety- and depressive-like) outcomes as a function of sex and age. Additionally, we detail a putative mechanistic role of PV on ELA-related outcomes and discuss evidence suggesting hormone influences on PV expression/function which may help to explain sex differences in ELA outcomes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Sex Differences in Affective Dysfunction and Alterations in Parvalbumin in Rodent Models of Early Life Adversity

Ellis

Ganguly

2021

Front. Behav. Neurosci.

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“…Several studies show decreased PNNs immediately after stress (Ueno et al, 2017;Pesarico et al, 2019;Gildawie et al, 2020Gildawie et al, , 2021Koskinen et al, 2020;Yu et al, 2020;Klimczak et al, 2021), and a rebound increase in PNNs as time passes following stress cessation (Dimatelis et al, 2013;Riga et al, 2017;Murthy et al, 2019;Koskinen et al, 2020;Gildawie et al, 2021). Although some findings do not fit with this summary (Page and Coutellier, 2018;Richardson et al, 2021), the majority of studies suggest a stress-induced trajectory involving first suppression followed by an overshooting rebound, similar to what has been observed for reelin signaling (Zhang et al, 2013). This is in line with other theories of stress effects on the ECM, particularly the idea that depressive-like symptoms emerge after an "incubation period, " which involves latent increases in PNNs and accompanying plasticity reduction (Koskinen et al, 2020;Spijker et al, 2020).…”

Section: Stress Effects On Perineuronal Netsmentioning

confidence: 81%

“…One study showed that postnatal stress using a scarcity/adversity model led to reduced PNN intensity in a subregion of the basolateral amygdala (Santiago et al, 2018), while another study using the same model reported increased PNN cell numbers but only on the right side of the amygdala in males (Guadagno et al, 2020). Two additional studies using maternal separation have reported either increased PNN intensity, but only in females (Gildawie et al, 2020), or no differences in PNN measures (Richardson et al, 2021). Although all of these studies used a similar method for identifying PNNs, they did not all use the same measure (WFA+ cell number vs. WFA intensity), and none used a label of a specific CSPG, such as aggrecan.…”

Section: Stress Effects On Perineuronal Netsmentioning

confidence: 99%

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

Laham

Gould

2022

Front. Cell. Neurosci.

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Diffuse and structured extracellular matrix (ECM) comprise ∼20% of the brain’s volume and play important roles in development and adult plasticity. Perineuronal nets (PNNs), specialized ECM structures that surround certain types of neurons in the brain, emerge during the postnatal period, making their development and maintenance potentially sensitive to experience. Recent studies have shown that stress affects diffuse ECM as well as PNNs, and that such effects are dependent on life stage and brain region. Given that the ECM participates in synaptic plasticity, the generation of neuronal oscillations, and synchronous firing across brain regions, all of which have been linked to cognition and emotional regulation, ECM components may be candidate therapeutic targets for stress-induced neuropsychiatric disease. This review considers the influence of stress over diffuse and structured ECM during postnatal life with a focus on functional outcomes and the potential for translational relevance.

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“… Gildawie et al (2020) , using repeated maternal separation in rats (4h per day from P2–P20), observed an increase in the density of PNNs in the BLA of adolescent males. By contrast, Richardson et al (2021) failed to replicate these findings, with a slightly different protocol of maternal separation (3h per day from P2–P14) in male and female rats ( Richardson et al, 2021 ). Using a limited bedding and nesting paradigm, which causes disruption of maternal care, male but not female adolescent rats presented an increased density of PNNs in the right BLA ( Guadagno et al, 2020 ).…”

Section: Impact Of Stress On Inhibitory Neuronsmentioning

confidence: 91%

Impact of stress on inhibitory neuronal circuits, our tribute to Bruce McEwen

Pérez-Rando

Carceller

Castillo-Gómez

et al. 2022

Neurobiology of Stress

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Does maternal separation accelerate maturation of perineuronal nets and parvalbumin-containing inhibitory interneurons in male and female rats?

Cited by 11 publications

References 57 publications

Sex Differences in Affective Dysfunction and Alterations in Parvalbumin in Rodent Models of Early Life Adversity

Sex Differences in Affective Dysfunction and Alterations in Parvalbumin in Rodent Models of Early Life Adversity

How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix

Impact of stress on inhibitory neuronal circuits, our tribute to Bruce McEwen

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