Region-specific effects of maternal separation on oxidative stress accumulation in parvalbumin neurons of male and female rats

Soares, Alexa R.; Gildawie, Kelsea R.; Ganguly, Prabarna; Brenhouse, Heather C.

doi:10.1016/j.bbr.2020.112658

Cited by 30 publications

(36 citation statements)

References 80 publications

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“…While altered PNN structural integrity in juvenility may have long term consequences on brain maturation, the current findings suggest that a second hit of juvenile adversity is required for prolonged PNN reduction in adulthood. Importantly, we have also found that PV cells in the PFC of juveniles exposed to neonatal MS undergo increased oxidative damage ( Soares et al, 2020 ). As degradation of PNNs via chondroitinase ABC has been found to increase PV neuron vulnerability to oxidative stress ( Cabungcal et al, 2013 ), this converging evidence suggests that a lack of PNNs following MS contributes to oxidative damage and consequential PV loss upon subsequent challenges.…”

Section: Discussionmentioning

confidence: 82%

A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior

Gildawie

Ryll

Hexter

et al. 2021

Developmental Cognitive Neuroscience

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Adversity early in life substantially impacts prefrontal cortex (PFC) development and vulnerability to later-life psychopathology. Importantly, repeated adverse experiences throughout childhood increase the risk for PFC-mediated behavioral deficits more commonly in women. Evidence from animal models points to effects of adversity on later-life neural and behavioral dysfunction; however, few studies have investigated the neurobiological underpinnings of sex-specific, long-term consequences of multiple developmental stressors. We modeled early life adversity in rats via maternal separation (postnatal day (P)2-20) and juvenile social isolation (P21-35). In adulthood, anxiety-like behavior was assessed in the elevated zero maze and the presence and structural integrity of PFC perineuronal nets (PNNs) enwrapping parvalbumin (PV)-expressing interneurons was quantified. PNNs are extracellular matrix structures formed during critical periods in postnatal development that play a key role in the plasticity of PV cells. We observed a female-specific effect of adversity on hyperactivity and risk-assessment behavior. Moreover, females – but not males – exposed to multiple hits of adversity demonstrated a reduction in PFC PV cells in adulthood. We also observed a sex-specific, potentiated reduction in PV + PNN structural integrity. These findings suggest a sex-specific impact of repeated adversity on neurostructural development and implicate PNNs as a contributor to associated behavioral dysfunction.

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Section: Discussionmentioning

confidence: 82%

A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior

Gildawie

Ryll

Hexter

et al. 2021

Developmental Cognitive Neuroscience

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“…However, it is important to also recognize the rapidly-growing body of work supporting changes in PNNs themselves (or their key components) in response to physiological stimuli, such as stress, exercise, environmental enrichment, diet, circadian rhythms, and normal aging processes. Short term and chronic stress lead to brain region-dependent changes in PV cells and PNNs both in early life (Castillo-Gómez et al, 2017 ; Ueno et al, 2018 ; Murthy et al, 2019 ; Guadagno et al, 2020 ; Soares et al, 2020 ; Yu et al, 2020 ) and in adults (Pesarico et al, 2019 ; Yu et al, 2020 ). Exercise also alters PNNs, and the effects are dependent on the brain region examined (Smith et al, 2015 ; Briones et al, 2021 ).…”

Section: Impact Of Physiological Stimuli On Pnnsmentioning

confidence: 99%

Impact of Perineuronal Nets on Electrophysiology of Parvalbumin Interneurons, Principal Neurons, and Brain Oscillations: A Review

Wingert

Sorg

2021

Front. Synaptic Neurosci.

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Perineuronal nets (PNNs) are specialized extracellular matrix structures that surround specific neurons in the brain and spinal cord, appear during critical periods of development, and restrict plasticity during adulthood. Removal of PNNs can reinstate juvenile-like plasticity or, in cases of PNN removal during early developmental stages, PNN removal extends the critical plasticity period. PNNs surround mainly parvalbumin (PV)-containing, fast-spiking GABAergic interneurons in several brain regions. These inhibitory interneurons profoundly inhibit the network of surrounding neurons via their elaborate contacts with local pyramidal neurons, and they are key contributors to gamma oscillations generated across several brain regions. Among other functions, these gamma oscillations regulate plasticity associated with learning, decision making, attention, cognitive flexibility, and working memory. The detailed mechanisms by which PNN removal increases plasticity are only beginning to be understood. Here, we review the impact of PNN removal on several electrophysiological features of their underlying PV interneurons and nearby pyramidal neurons, including changes in intrinsic and synaptic membrane properties, brain oscillations, and how these changes may alter the integration of memory-related information. Additionally, we review how PNN removal affects plasticity-associated phenomena such as long-term potentiation (LTP), long-term depression (LTD), and paired-pulse ratio (PPR). The results are discussed in the context of the role of PV interneurons in circuit function and how PNN removal alters this function.

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“…Their higher sensitivity to oxidative stress might also make them more vulnerable to other types of stress from the environment. This is illustrated in a recent study showing changes in PV staining intensity, but not PV neuron numbers in the amygdala after early maternal separation in adult male and female rats ( Gildawie et al, 2020a ; Soares et al, 2020 ). It is interesting to note that in this particular study, maternal separation did not change PV staining intensity or cell number in the mPFC or in subfields of the hippocampus of either males or females, suggesting that effects on PV-INs are region-specific.…”

Section: Early Life Stress Modulates Local Amygdala Circuits and Inhibitory Interneuronsmentioning

confidence: 90%

Effects of Early Life Stress on the Developing Basolateral Amygdala-Prefrontal Cortex Circuit: The Emerging Role of Local Inhibition and Perineuronal Nets

Guadagno

Belliveau

Mechawar

et al. 2021

Front. Hum. Neurosci.

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The links between early life stress (ELS) and the emergence of psychopathology such as increased anxiety and depression are now well established, although the specific neurobiological and developmental mechanisms that translate ELS into poor health outcomes are still unclear. The consequences of ELS are complex because they depend on the form and severity of early stress, duration, and age of exposure as well as co-occurrence with other forms of physical or psychological trauma. The long term effects of ELS on the corticolimbic circuit underlying emotional and social behavior are particularly salient because ELS occurs during critical developmental periods in the establishment of this circuit, its local balance of inhibition:excitation and its connections with other neuronal pathways. Using examples drawn from the human and rodent literature, we review some of the consequences of ELS on the development of the corticolimbic circuit and how it might impact fear regulation in a sex- and hemispheric-dependent manner in both humans and rodents. We explore the effects of ELS on local inhibitory neurons and the formation of perineuronal nets (PNNs) that terminate critical periods of plasticity and promote the formation of stable local networks. Overall, the bulk of ELS studies report transient and/or long lasting alterations in both glutamatergic circuits and local inhibitory interneurons (INs) and their associated PNNs. Since the activity of INs plays a key role in the maturation of cortical regions and the formation of local field potentials, alterations in these INs triggered by ELS might critically participate in the development of psychiatric disorders in adulthood, including impaired fear extinction and anxiety behavior.

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Region-specific effects of maternal separation on oxidative stress accumulation in parvalbumin neurons of male and female rats

Cited by 30 publications

References 80 publications

A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior

A two-hit adversity model in developing rats reveals sex-specific impacts on prefrontal cortex structure and behavior

Impact of Perineuronal Nets on Electrophysiology of Parvalbumin Interneurons, Principal Neurons, and Brain Oscillations: A Review

Effects of Early Life Stress on the Developing Basolateral Amygdala-Prefrontal Cortex Circuit: The Emerging Role of Local Inhibition and Perineuronal Nets

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