Effects of central and peripheral inflammation on hippocampal synaptic plasticity

Filippo, Massimiliano Di; Chiasserini, Davide; Gardoni, Fabrizio; Viviani, Bárbara; Tozzi, Alessandro; Giampà, Carmela; Costa, Cinzia; Tantucci, Michela; Zianni, Elisa; Boraso, Mariaserena; Siliquini, Sabrina; Iure, Antonio de; Ghiglieri, Veronica; Colcelli, Elisa; Baker, David; Sarchielli, Paola; Fusco, Francesca R.; Luca, Monica Di; Calabresi, Paolo

doi:10.1016/j.nbd.2012.12.009

Cited by 160 publications

(121 citation statements)

References 44 publications

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“…27 During systemic or central nervous system inflammation, the modulation exerted by neuroinflammatory mediators on synaptic plasticity might negatively or positively influence brain neuronal networks functioning. 28 Activation of a cytokine network in the brain is a physiologic relevant phenomenon not only for long-term potentiation maintenance, but also for certain types of learning. 29 Interfering with cytokine signaling can either inhibit or support long-term potentiation maintenance.…”

Section: Perioperative Sf Enhanced the Neuroinflammatory Response To mentioning

confidence: 99%

Fragmented Sleep Enhances Postoperative Neuroinflammation but Not Cognitive Dysfunction

Vacas

Degos

Maze

2017

Anesthesia &Amp; Analgesia

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BACKGROUND: Sleep is integral to biologic function, and sleep disruption can result in both physiological and psychologic dysfunction including cognitive decline. Surgery activates the innate immune system, inducing neuroinflammatory changes that interfere with cognition. Because surgical patients with sleep disorders have an increased likelihood of exhibiting postoperative delirium, an acute form of cognitive decline, we investigated the contribution of perioperative sleep fragmentation (SF) to the neuroinflammatory and cognitive responses of surgery. METHODS: The effects of 24-hour SF and surgery were explored in adult C57BL/6J male mice. The SF procedure started at 7 am with cages being placed on a large platform orbital shaker that cycled every 120 seconds (30 seconds on/90 seconds off) for 24 hours. In separate cohorts, stabilized tibial fracture was performed either before or after the 24-hour SF procedure and assessed for systemic and hippocampal inflammation and cognition. RESULTS: SF-induced nonhippocampal memory dysfunction (mean ± standard deviation [SD] of the difference in time spent between novel and familiar object for control was 4.7 ± 1.4 seconds, n = 8 versus SF −0.5 ± 0.2 seconds, n = 11, yielding an estimated treatment effect of 5.2 seconds [95% confidence interval {CI}, 2.6–7.7]; P < .001) and increased systemic interleukin-6 (median [25%–75% quartile] for control 0.0 [0.0–2.4] pg/mL versus 9.7 [6.3–12.9] pg/mL, n = 8/group, yielding an estimated treatment effect of 9.7 pg/mL [95% CI, 5.8–11.8]; P < .0001). SF reduced freezing time in hippocampal-dependent memory test (mean ± SD for control 49.3% ± 5.8% versus for SF 32.9% ± 5.8%, n = 10/group, estimated treatment effect = 16.4% [95% CI, 11.0–21.8]; P < .0001). Although surgery also reduced freezing time (mean ± SD for control 49.3% ± 5.8% versus for surgery 30.3% ± 3.3%, n = 10/group, estimated treatment effect = 19.0% [95% CI, 14.6–23.4]; P < .0001), memory impairment was not further exacerbated by combining SF with surgery. One day after SF, there was an increase in hippocampal messenger RNA expression of tumor necrosis factor-α (relative quantitation [RQ] 5.12-fold, n = 5/group [95% CI, 1.64–15.97]; P < .01), and 1 day after surgery, there was an increase in messenger RNA interleukin-6 (RQ 4.64-fold, n = 5 [95% CI, 1.48–14.56]; P < .05) and tumor necrosis factor-α (RQ 5.54-fold, n = 5 [95% CI, 2.92–10.51]; P < .01). These increments were more pronounced when either pre- or postoperative SF was combined with surgery. CONCLUSIONS: Although SF and surgery can independently produce significant memory impairment, perioperative SF significantly increased hippocampal inflammation without further cognitive impairment. The dissociation between neuroinflammation and cognitive decline may relate to the use of a sole memory paradigm that does not capture other aspects of cognition, especially learning.

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Section: Perioperative Sf Enhanced the Neuroinflammatory Response To mentioning

confidence: 99%

Fragmented Sleep Enhances Postoperative Neuroinflammation but Not Cognitive Dysfunction

Vacas

Degos

Maze

2017

Anesthesia &Amp; Analgesia

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“…Other research groups confirmed this evidence, suggesting a key role for this cytokine in synaptic plasticity defects observed during neuroinflammatory processes [58,66,[68][69][70]. However, endogenous IL-1β is normally expressed at low levels in control conditions, and it has been proposed to be essential for the physiological induction of hippocampal LTP and consolidation of memory [65,71].…”

Section: Microglia Neuroinflammation and Synaptic Plasticity: A Deepmentioning

confidence: 84%

“…In our laboratory, we found an impaired LTP induction in the hippocampal CA1 area both during the acute inflammatory peak phase of EAE [68] and the later remission phase [58]. As experimental model for MS, we induced EAE in Biozzi ABH mice, which are particularly prone to develop autoimmune responses, by the injection of syngeneic spinal cord homogenate [68].…”

Section: Hippocampal Synaptic Plasticity In Experimental Models Of Msmentioning

confidence: 99%

“…As experimental model for MS, we induced EAE in Biozzi ABH mice, which are particularly prone to develop autoimmune responses, by the injection of syngeneic spinal cord homogenate [68]. This model follows a clinical course, reminiscent of relapsingremitting MS, with acute phases characterized by detectable neurological signs followed by remissions with partial or complete recovery, with a later progressive phase [76].…”

Section: Hippocampal Synaptic Plasticity In Experimental Models Of Msmentioning

confidence: 99%

“…This model follows a clinical course, reminiscent of relapsingremitting MS, with acute phases characterized by detectable neurological signs followed by remissions with partial or complete recovery, with a later progressive phase [76]. During the first acute relapse of EAE, the LTP impairment was found to be associated with an intense activation of hippocampal microglia and an increased hippocampal concentration of IL-1β [68]. Such hippocampal synaptic plasticity disruption was associated with changes in the subunit composition of NMDA glutamate receptor in the hippocampus, with a reduced expression of GluN2B-subunit [68].…”

Section: Hippocampal Synaptic Plasticity In Experimental Models Of Msmentioning

confidence: 99%

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Hippocampal neuroplasticity and inflammation: relevance for multiple sclerosis

Mancini

Gaetani

Gregorio

et al. 2017

Mult Scler Demyelinating Disord

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Cognitive impairment is very frequent during multiple sclerosis (MS), involving approximately 40-70% of the patients, with a profound impact on patient's life. It is now established that among the various central nervous system (CNS) structures involved during the course of MS, the hippocampus is particularly sensitive to the detrimental effects of neuroinflammation. Different studies demonstrated hippocampal involvement during MS, in association with depression and cognitive impairment, such as verbal and visuo-spatial memory deficits, even during the earlier phases of the disease. These cognitive alterations could represent the visible consequences of a hidden synaptic impairment. Indeed, neuronal and immune functions are intertwined and the immune system is able to modulate the efficacy of synaptic transmission and the induction of the main forms of synaptic plasticity, such as long term potentiation (LTP). Hippocampal synaptic plasticity has been studied during the last decades as the physiological basis of human learning and memory and its disruption can be associated with behavioral and cognitive abnormalities. The aim of the present work is to review the available evidence about the presence of hippocampal synaptic plasticity alterations in experimental models of MS, specifically during the course of experimental autoimmune encephalomyelitis (EAE) and to discuss their relevance with regard to human MS. Indeed, the failure of synapses to express plasticity during neuroinflammation could potentially lead to a progressive failure of the brain plastic reserve, possibly contributing to disability progression and cognitive impairment during MS.

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Effect of Agomelatine and Fluoxetine on HAM‐D Score, Serum Brain‐Derived Neurotrophic Factor, and Tumor Necrosis Factor‐α Level in Patients With Major Depressive Disorder With Severe Depression

Gupta

Bhatia

et al. 2017

The Journal of Clinical Pharma

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Evidence suggests that neurotrophic factors, inflammatory markers, and circadian rhythm dysfunctions could be involved in pathophysiology of major depressive disorder. This study evaluated the efficacy and tolerability of agomelatine, a melatonergic drug, and fluoxetine (positive comparator) and their effect on serum brain-derived neurotrophic factor (BDNF) and tumor necrosis factor (TNF)-α level in patients having major depressive disorder with severe depression. In the present study, we chose TNF-α and BDNF because reduction of TNF-α and rise in BDNF levels are linked with improvement in major depressive disorder. Patients with Hamilton Rating Scale for Depression (HAM-D) score ≥25 were treated with agomelatine or fluoxetine and followed up for 12 weeks. In the agomelatine group, the HAM-D score, BDNF level, and TNF-α level at the start of treatment were 31.1 ± 1.88 ng/mL, 2.44 ± 0.38 ng/mL, and 512.5 ± 86.2 pg/mL, respectively, which significantly changed to 13.67 ± 2.22 ng/mL, 2.87 ± 0.44 ng/mL, and 391.64 ± 104.8 pg/mL, respectively (P < .05 for all 3 measures), at 12 weeks. In the fluoxetine group, the HAM-D score, BDNF level, and TNF-α level at the start of treatment were 30.83 ± 2.60 ng/mL, 2.54 ± 0.37 ng/mL, and 554.14 ± 46.8 pg/mL, respectively, which significantly changed to 13.67 ± 1.79 ng/mL, 3.07 ± 0.33 ng/mL, and 484.15 ± 49.9 pg/mL, respectively (P < .05 for all 3 measures) at 12 weeks. The BDNF level was significantly increased posttreatment with both drugs, and TNF-α level fell significantly more with agomelatine compared to fluoxetine. Thus, chronic neuroinflammatory biomarkers contribute to circuitry dysregulation in depression. Trophic factors repair dysfunctional circuits in depression. Both treatments were found to be safe and well tolerated.

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Effects of central and peripheral inflammation on hippocampal synaptic plasticity

Cited by 160 publications

References 44 publications

Fragmented Sleep Enhances Postoperative Neuroinflammation but Not Cognitive Dysfunction

Fragmented Sleep Enhances Postoperative Neuroinflammation but Not Cognitive Dysfunction

Hippocampal neuroplasticity and inflammation: relevance for multiple sclerosis

Effect of Agomelatine and Fluoxetine on HAM‐D Score, Serum Brain‐Derived Neurotrophic Factor, and Tumor Necrosis Factor‐α Level in Patients With Major Depressive Disorder With Severe Depression

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