Incubation of depression: ECM assembly and parvalbumin interneurons after stress

Spijker, Sabine; Koskinen, Maija-Kreetta; Riga, Danai

doi:10.1016/j.neubiorev.2020.07.015

Cited by 33 publications

(38 citation statements)

References 155 publications

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“…Our studies suggest that PNFlx treatment, which evokes persistent increases in anxiety-and despair-like behavior across the life-span, also targets the formation of PNNs in the hippocampus, a brain region implicated in the regulation of mood-related behavior. A disruption of molecular and cellular regulators of critical period plasticity during postnatal maturation has been suggested to be a common signature associated with animal models of depression, based on early adversity exposure, as well as genetic and pharmacological models of neurodevelopmental disorders (Callaghan et al, 2013;Do et al, 2015;Fagiolini & Leblanc, 2011;Spijker et al, 2020). PNN formation and maturation marks the end of the critical period plasticity window in most circuits, and a delay in PNN maturation is suggestive of a protracted closure of the critical period (Hensch, 2005).…”

Section: Discussionmentioning

confidence: 99%

Postnatal fluoxetine treatment alters perineuronal net formation and maintenance in the hippocampus

Mukhopadhyay

Chatterjee

Tiwari

et al. 2020

Preprint

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Elevation of serotonin via postnatal fluoxetine (PNFlx) treatment during critical temporal windows is hypothesized to perturb the development of limbic circuits thus establishing a substratum for persistent disruption of mood-related behavior. We examined the impact of PNFlx treatment on the formation and maintenance of perineuronal nets (PNNs), extracellular matrix (ECM) structures that deposit primarily around inhibitory interneurons, and mark the closure of critical period plasticity. PNFlx treatment evoked a significant decline in PNN number, with a robust reduction in PNNs deposited around parvalbumin (PV) interneurons, within the CA1 and CA3 hippocampal subfields at postnatal day 21 in Sprague-Dawley rat pups. While the reduction in CA1 subfield PNN number was still observed in adulthood, we observed no change in colocalization of PV-positive interneurons with PNNs in the hippocampi of adult PNFlx animals. PNFlx treatment did not alter hippocampal parvalbumin, calretinin, or reelin-positive neuron numbers in PNFlx animals at P21 or in adulthood. We did observe a small, but significant increase in somatostatin (SST)-positive interneurons in the DG subfield of PNFlx-treated animals in adulthood. This was accompanied by altered GABA-A receptor subunit composition, increased dendritic complexity of apical dendrites of CA1 pyramidal neurons, and enhanced neuronal activation revealed by increased c-Fos-positive cell numbers within hippocampi of PNFlx-treated animals in adulthood. These results indicate that PNFlx treatment alters the developmental trajectory of PNNs within the hippocampus, raising the possibility of a disruption of critical period plasticity and the establishment of an altered excitation-inhibition balance within this key limbic brain region.

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Section: Discussionmentioning

confidence: 99%

Postnatal fluoxetine treatment alters perineuronal net formation and maintenance in the hippocampus

Mukhopadhyay

Chatterjee

Tiwari

et al. 2020

Preprint

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“…PNNs preferentially surround Pv-FSI both are subject to change after exposure to stress, therefore possibly impairing the Pvnetworks throughout the brain. A review of studies that have examined these relationships using many different behavioral models of stress and at different time points (prenatal, early and late adolescence, adulthood etc.,), levels of exposure, and trajectories, have consistently shown that stress results in changes in PNN-Pv density (54).…”

Section: Pv-fsi Regulation In Human Neurological Diseasementioning

confidence: 92%

“…Another interesting aspect of Pv interneurons in the brain is the connections they form with cellular structures. Several studies have shown that Pv-related psychiatric diseases induce changes in cell structures like the extracellular matrix (ECM) and perineuronal nets (PNN) across several brain regions (54). PNNs preferentially surround Pv-FSI both are subject to change after exposure to stress, therefore possibly impairing the Pvnetworks throughout the brain.…”

Section: Pv-fsi Regulation In Human Neurological Diseasementioning

confidence: 99%

The Role of Parvalbumin Interneurons in Neurotransmitter Balance and Neurological Disease

2021

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While great progress has been made in the understanding of neurological illnesses, the pathologies, and etiologies that give rise to these diseases still remain an enigma, thus, also making treatments for them more challenging. For effective and individualized treatment, it is beneficial to identify the underlying mechanisms that govern the associated cognitive and behavioral processes that go awry in neurological disorders. Parvalbumin fast-spiking interneurons (Pv-FSI) are GABAergic cells that are only a small fraction of the brain's neuronal network, but manifest unique cellular and molecular properties that drastically influence the downstream effects on signaling and ultimately change cognitive behaviors. Proper brain functioning relies heavily on neuronal communication which Pv-FSI regulates, excitatory-inhibitory balances and GABAergic disinhibition between circuitries. This review highlights the depth of Pv-FSI involvement in the cortex, hippocampus, and striatum, as it pertains to expression, neurotransmission, role in neurological disorders, and dysfunction, as well as cognitive behavior and reward-seeking. Recent research has indicated that Pv-FSI play pivotal roles in the molecular pathophysiology and cognitive-behavioral deficits that are core features of many psychiatric disorders, such as schizophrenia, autism spectrum disorders, Alzheimer's disease, and drug addiction. This suggests that Pv-FSI could be viable targets for treatment of these disorders and thus calls for further examination of the undeniable impact Pv-FSI have on the brain and cognitive behavior.

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“…One novel adaptation of subordination stress is the social defeat-prolonged stress (SDPS) paradigm, in which an animal is subordinated to another for five consecutive days and then socially isolated until testing. This manipulation is meant to mimic a traumatic trigger and the following lack of social support that is associated with depression ( Spijker et al., 2020 ). Some other chronic stress paradigms used in rodents include chronic mild stress, chronic variable stress (CVS), and unpredictable chronic mild stress (UCMS) ( Spijker et al., 2020 ).…”

Section: Methodsmentioning

confidence: 99%

“…This manipulation is meant to mimic a traumatic trigger and the following lack of social support that is associated with depression ( Spijker et al., 2020 ). Some other chronic stress paradigms used in rodents include chronic mild stress, chronic variable stress (CVS), and unpredictable chronic mild stress (UCMS) ( Spijker et al., 2020 ). These involve subjecting rodents to a variety of stressors, typically physical or social.…”

Section: Methodsmentioning

confidence: 99%

Parvalbumin interneuron alterations in stress-related mood disorders: A systematic review

Perlman¹,

Tanti²,

Mechawar³

2021

Neurobiology of Stress

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Stress-related psychiatric disorders including depression involve complex cellular and molecular changes in the brain, and GABAergic signaling dysfunction is increasingly implicated in the etiology of mood disorders. Parvalbumin (PV)-expressing neurons are fast-spiking interneurons that, among other roles, coordinate synchronous neuronal firing. Mounting evidence suggests that the PV neuron phenotype is altered by stress and in mood disorders. In this systematic review, we assessed PV interneuron alterations in psychiatric disorders as reported in human postmortem brain studies and animal models of environmental stress. This review aims to 1) comprehensively catalog evidence of PV cell function in mood disorders (humans) and stress models of mood disorders (animals); 2) analyze the strength of evidence of PV interneuron alterations in various brain regions in humans and rodents; 3) determine whether the modulating effect of antidepressant treatment, physical exercise, and environmental enrichment on stress in animals associates with particular effects on PV function; and 4) use this information to guide future research avenues. Its principal findings, derived mainly from rodent studies, are that stress-related changes in PV cells are only reported in a minority of studies, that positive findings are region-, age-, sex-, and stress recency-dependent, and that antidepressants protect from stress-induced apparent PV cell loss. These observations do not currently translate well to humans, although the postmortem literature on the topic remains limited.

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Incubation of depression: ECM assembly and parvalbumin interneurons after stress

Cited by 33 publications

References 155 publications

Postnatal fluoxetine treatment alters perineuronal net formation and maintenance in the hippocampus

Postnatal fluoxetine treatment alters perineuronal net formation and maintenance in the hippocampus

The Role of Parvalbumin Interneurons in Neurotransmitter Balance and Neurological Disease

Parvalbumin interneuron alterations in stress-related mood disorders: A systematic review

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