Neonatal maternal separation leads to a dampening of inflammation-related mechanical and thermal hypersensitivity in juvenile rats

Genty, Julien; Nomigni, Milène Tetsi; Anton, Fernand; Hanesch, Ulrike

doi:10.1016/j.neulet.2018.03.044

Cited by 6 publications

(6 citation statements)

References 33 publications

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“…While this blunting of expression was not predicted, it also is not without precedent. Early-life social separation was found to reduce later peripheral inflammatory response to LPS in mice, rats, and piglets (Avitsur et al, 2013;Roque et al, 2016;Saavedra et al, 2018;Tuchscherer et al, 2004), and later inflammatory pain sensitivity in rats (Genty et al, 2018). As for the CNS, prenatal exposure to alcohol reduced hypothalamic levels of IL-1β, TNF-α, and IL-6 in preweaning rats (Bodnar, 2017), and earlier separation reduced the TNF-α response, though increased the IL-1β response, to LPS in the hippocampus of piglets (Tuchscherer et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Central neuroimmune activity and depressive-like behavior in response to repeated maternal separation and injection of LPS

Hennessy

Deak

Sensenbaugh

et al. 2019

Physiology & Behavior

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Disruption of attachment relations in early life is linked to greater vulnerability to depressive illness at later ages. Evidence suggests this process involves stress-induced activation of central inflammatory factors, though the specific mediators and processes involved are not known. We used a guinea pig model in which effects of maternal separation appear more clearly due to absence of the attachment figure than is the case for other laboratory rodents. Separation in a novel environment on two consecutive days evoked a depressive-like behavioral response that sensitized during a final test 9 days later. At this time, prior separation blunted the response of prostaglandin synthesizing enzymes (COX-2 and mPGES) and chemokines (CXCL-1 and MCP-1) 120 min following injection with lipopolysaccharide and isolation in a novel cage. The blunted response was not associated with a greater plasma cortisol elevation. In addition, injection of saline just prior to isolation at the oldest age elicited small, but significant, elevations in several signaling molecules, particularly at 30 min. These results demonstrate lasting central inflammatory consequences of our separation procedure. However, contrary to expectations, sensitization of depressive-like behavior was not associated with an increase in expression of neuroimmune mediators to inflammatory challenge. Together with earlier findings, the results suggest a multistep process in which inflammatory response to an initial separation affects downstream mediators to sensitize depressive-like behavior.

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Section: Discussionmentioning

confidence: 99%

Central neuroimmune activity and depressive-like behavior in response to repeated maternal separation and injection of LPS

Hennessy

Deak

Sensenbaugh

et al. 2019

Physiology & Behavior

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“…We previously studied the effects of MS, an established ELS paradigm on the development of neuropathic [ 10 ] and inflammatory pain [ 11 ] in adult age. While these studies revealed that MS may be beneficial, in the sense that it promotes a form of resilience against pain hypersensitivity, other studies showed that MS can lead to an enhanced vulnerability to chronic pain conditions [ 34 , 35 ].…”

Section: Discussionmentioning

confidence: 99%

“…The spinal cord is however of major importance since it constitutes the point of entry and distribution of noxious information throughout the central nervous system [ 9 ]. We previously observed that maternal separation (MS), a rodent model of ELS could per se have a beneficial effect regarding the establishment of neuropathy- and inflammation-induced hyperalgesia in later life [ 10 , 11 ].…”

Section: Introductionmentioning

confidence: 99%

The combination of postnatal maternal separation and social stress in young adulthood does not lead to enhanced inflammatory pain sensitivity and depression-related behavior in rats

et al. 2018

Self Cite

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The cumulative and match/mismatch hypotheses of stress are still under discussion regarding the effects of early life stress (ELS) on the vulnerability or resilience to psychopathology. In this context, an additional stress in later life (second hit) often leads to stress-related disorders that frequently include comorbid pain states. We previously observed that maternal separation (MS), a model of ELS, reduces vulnerability to neuropathic and inflammatory pain in rats. In the present study, we investigated the effects of an additional later stressor on the vulnerability to inflammatory pain. Sprague Dawley pups were divided into 4 groups: controls (CON, no stress), MS, social stress (SS) and MS+SS. At young adult age (from 7 to 15 weeks), stress- as well as pain-related parameters were evaluated prior and during 21 days following the induction of paw inflammation with complete Freund’s adjuvant (CFA). Finally spinal glutamatergic transmission, immunocompetent cells, pro-inflammatory cytokines and growth factors were examined using qPCR. None of the stress conditions had a significant impact on corticosterone levels and anhedonia. In the forced swim test, MS and SS displayed increased passive coping whereas the combination of both stressors revoked this effect. The different stress conditions had no influence on basal mechanical thresholds and heat sensitivity. At 4 days post-inflammation all stress groups displayed lower mechanical thresholds than CON but the respective values were comparable at 7, 10, and 14 days. Only on day 21, MS rats were more sensitive to mechanical stimulation compared to the other groups. Regarding noxious heat sensitivity, MS+SS animals were significantly less sensitive than CON at 10 and 21 days after CFA-injection. qPCR results were mitigated. Despite the finding that stress conditions differentially affected different players of glutamatergic transmission, astrocyte activity and NGF expression, our biochemical results could not readily be related to the behavioral observations, precluding a congruent conclusion. The present results do neither confirm the cumulative nor corroborate or disprove the match/mismatch hypothesis.

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“…Studies have suggested that ELS is a potent mediator of nociception, altering sensitivity to painful stimuli derived from inflammatory conditions in adulthood. Genty et al (2018) observed that ELS reduced the hyperalgesia caused by the injection of Complete Freunds Adjuvant (CFA) an immunostimulatory substance (Genty et al, 2018). Lower sensitivity to pain was also observed after rats previously exposed to ELS have been subjected to a second stressful stimulus in adulthood (Post et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Early life stress exacerbates bone resorption and inhibits anxiety‐like behaviour induced by apical periodontitis in rats

et al. 2022

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Aim To evaluate the influence of the early life stress (ELS) on the severity of the apical periodontitis (AP) in Wistar rats. Methodology Forty male Wistar rats were divided into four groups (n = 10): Control rats; AP—rats with AP; ELS—rats subject to ELS; AP + ELS—rats exposed to ELS and subject to AP. ELS was induced by maternal separation (MS) for a period of 3 h for 21 consecutive days. AP was induced via pulp exposure of the first and second right maxillary molars to the oral environment for 40 days. Three days before euthanasia, all rats underwent behavioural analysis to measure anxiety levels by elevated zero maze. Then, the rats were euthanized and the maxillas were removed to assess the occurrence and severity of AP. The periapical region was evaluated for the intensity of the inflammatory infiltrate and the extent of bone loss. The Mann–Whitney test was performed for nonparametric data, and the Tukey's or Student's t‐test was performed for parametric data (p < .05). Results The intensity of the inflammatory infiltrate was significantly larger in the AP + ELS group when compared with AP group (p < .05). The AP + ELS group exhibited significantly greater alveolar bone loss, with a periapical lesion size of 103.5 ± 29.88, compared with 72.3 ± 22.28 in the AP group (p < .05). Rats with AP displayed higher anxiety‐like behaviour in relation to the control group (p < .05). However, exposure to ELS abolished the AP‐induced increased anxiety‐like ‘behaviour’ throughout, since that rats from AP + ELS group attended more the open arms than non‐stressed rats with AP (p < .05). Conclusion Early life stress is predictive of the severity of AP exacerbating the inflammatory process and increasing periapical bone resorption.

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Neonatal maternal separation leads to a dampening of inflammation-related mechanical and thermal hypersensitivity in juvenile rats

Cited by 6 publications

References 33 publications

Central neuroimmune activity and depressive-like behavior in response to repeated maternal separation and injection of LPS

Central neuroimmune activity and depressive-like behavior in response to repeated maternal separation and injection of LPS

The combination of postnatal maternal separation and social stress in young adulthood does not lead to enhanced inflammatory pain sensitivity and depression-related behavior in rats

Early life stress exacerbates bone resorption and inhibits anxiety‐like behaviour induced by apical periodontitis in rats

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