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CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment.

Maggi L, Scianni M, Branchi I, D'Andrea I, Lauro C, Limatola C - Front Cell Neurosci (2011)

Bottom Line: At this aim wt and CX(3)CR1(GFP/GFP) mice were exposed to long-lasting-enriched environment (EE) and the effects on hippocampal functions were studied by electrophysiological recordings of long-term potentiation of synaptic activity, behavioral tests of learning and memory in the Morris water maze paradigm and analysis of neurogenesis in the subgranular zone of the dentate gyrus (DG).We found that CX(3)CR1 deficiency increases hippocampal plasticity and spatial memory, blunting the potentiating effects of EE.These data indicate that CX(3)CL1/CX(3)CR1-mediated signaling is crucial for a normal experience-dependent modulation of hippocampal functions.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, Istituto Pasteur Fondazione Cenci Bolognetti, Università di Roma Rome Italy.

ABSTRACT
In recent years several evidence demonstrated that some features of hippocampal biology, like neurogenesis, synaptic transmission, learning, and memory performances are deeply modulated by social, motor, and sensorial experiences. Fractalkine/CX(3)CL1 is a transmembrane chemokine abundantly expressed in the brain by neurons, where it modulates glutamatergic transmission and long-term plasticity processes regulating the intercellular communication between glia and neurons, being its specific receptor CX(3)CR1 expressed by microglia. In this paper we investigated the role of CX(3)CL1/CX(3)CR1 signaling on experience-dependent hippocampal plasticity processes. At this aim wt and CX(3)CR1(GFP/GFP) mice were exposed to long-lasting-enriched environment (EE) and the effects on hippocampal functions were studied by electrophysiological recordings of long-term potentiation of synaptic activity, behavioral tests of learning and memory in the Morris water maze paradigm and analysis of neurogenesis in the subgranular zone of the dentate gyrus (DG). We found that CX(3)CR1 deficiency increases hippocampal plasticity and spatial memory, blunting the potentiating effects of EE. In contrast, exposure to EE increased the number and migration of neural progenitors in the DG of both wt and CX(3)CR1(GFP/GFP) mice. These data indicate that CX(3)CL1/CX(3)CR1-mediated signaling is crucial for a normal experience-dependent modulation of hippocampal functions.

No MeSH data available.


Related in: MedlinePlus

CA1 plasticity of wt and CX3CR1GFP/GFP mice exposed either to SE or EE conditions. Points represent mean ± SEM. Of fEPSP slopes evoked every 20 s and normalized as detailed in the Section “Materials and Methods.” Arrows indicate time of application of HFS. (A) Enhancement of LTP in wt mice raised in EE: 45 min after HFS, EE wt mice (open circle) developed a robust LTP of fEPSP slope compared to that of mice raised in SE (dark square, p < 0.001). (B) In CX3CR1GFP/GFP mice LTP is enhanced and EE produced no effect: after HFS, the amplitude of fEPSP potentiation of EE CX3CR1GFP/GFP mice (open circle) is not different from that obtained in SE mice (dark square). Note that that basal LTP evoked in SE is increased in CX3CR1GFP/GFP mice compared to wt [in (A), p = 0.006].
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Figure 1: CA1 plasticity of wt and CX3CR1GFP/GFP mice exposed either to SE or EE conditions. Points represent mean ± SEM. Of fEPSP slopes evoked every 20 s and normalized as detailed in the Section “Materials and Methods.” Arrows indicate time of application of HFS. (A) Enhancement of LTP in wt mice raised in EE: 45 min after HFS, EE wt mice (open circle) developed a robust LTP of fEPSP slope compared to that of mice raised in SE (dark square, p < 0.001). (B) In CX3CR1GFP/GFP mice LTP is enhanced and EE produced no effect: after HFS, the amplitude of fEPSP potentiation of EE CX3CR1GFP/GFP mice (open circle) is not different from that obtained in SE mice (dark square). Note that that basal LTP evoked in SE is increased in CX3CR1GFP/GFP mice compared to wt [in (A), p = 0.006].

Mentions: It has been reported that hippocampal LTP, induced by a weak stimulation (1 s burst of 100 Hz, HFS) in the CA1 region of the hippocampus, is enhanced by enrichment (Duffy et al., 2001). Following the same protocol of induction, we measured fEPSP potentiation in hippocampal slices in wt and CX3CR1GFP/GFP mice following exposure to either SE or EE (Figure 1A,B). In wt mice, the mean fEPSP slope potentiation, measured 35–45 min after LTP induction, was 1.05 ± 0.04 (17 slices/8 mice) and 1.56 ± 0.08 of baseline (17 slices/9 mice) in SE and EE, respectively. In CX3CR1GFP/GFP mice, LTP induction produced fEPSP slope potentiation of 1.19 ± 0.06 (17 slices/7 mice) and 1.26 ± 0.07 (27 slices/9 mice) in SE and EE, respectively.


CX(3)CR1 deficiency alters hippocampal-dependent plasticity phenomena blunting the effects of enriched environment.

Maggi L, Scianni M, Branchi I, D'Andrea I, Lauro C, Limatola C - Front Cell Neurosci (2011)

CA1 plasticity of wt and CX3CR1GFP/GFP mice exposed either to SE or EE conditions. Points represent mean ± SEM. Of fEPSP slopes evoked every 20 s and normalized as detailed in the Section “Materials and Methods.” Arrows indicate time of application of HFS. (A) Enhancement of LTP in wt mice raised in EE: 45 min after HFS, EE wt mice (open circle) developed a robust LTP of fEPSP slope compared to that of mice raised in SE (dark square, p < 0.001). (B) In CX3CR1GFP/GFP mice LTP is enhanced and EE produced no effect: after HFS, the amplitude of fEPSP potentiation of EE CX3CR1GFP/GFP mice (open circle) is not different from that obtained in SE mice (dark square). Note that that basal LTP evoked in SE is increased in CX3CR1GFP/GFP mice compared to wt [in (A), p = 0.006].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198035&req=5

Figure 1: CA1 plasticity of wt and CX3CR1GFP/GFP mice exposed either to SE or EE conditions. Points represent mean ± SEM. Of fEPSP slopes evoked every 20 s and normalized as detailed in the Section “Materials and Methods.” Arrows indicate time of application of HFS. (A) Enhancement of LTP in wt mice raised in EE: 45 min after HFS, EE wt mice (open circle) developed a robust LTP of fEPSP slope compared to that of mice raised in SE (dark square, p < 0.001). (B) In CX3CR1GFP/GFP mice LTP is enhanced and EE produced no effect: after HFS, the amplitude of fEPSP potentiation of EE CX3CR1GFP/GFP mice (open circle) is not different from that obtained in SE mice (dark square). Note that that basal LTP evoked in SE is increased in CX3CR1GFP/GFP mice compared to wt [in (A), p = 0.006].
Mentions: It has been reported that hippocampal LTP, induced by a weak stimulation (1 s burst of 100 Hz, HFS) in the CA1 region of the hippocampus, is enhanced by enrichment (Duffy et al., 2001). Following the same protocol of induction, we measured fEPSP potentiation in hippocampal slices in wt and CX3CR1GFP/GFP mice following exposure to either SE or EE (Figure 1A,B). In wt mice, the mean fEPSP slope potentiation, measured 35–45 min after LTP induction, was 1.05 ± 0.04 (17 slices/8 mice) and 1.56 ± 0.08 of baseline (17 slices/9 mice) in SE and EE, respectively. In CX3CR1GFP/GFP mice, LTP induction produced fEPSP slope potentiation of 1.19 ± 0.06 (17 slices/7 mice) and 1.26 ± 0.07 (27 slices/9 mice) in SE and EE, respectively.

Bottom Line: At this aim wt and CX(3)CR1(GFP/GFP) mice were exposed to long-lasting-enriched environment (EE) and the effects on hippocampal functions were studied by electrophysiological recordings of long-term potentiation of synaptic activity, behavioral tests of learning and memory in the Morris water maze paradigm and analysis of neurogenesis in the subgranular zone of the dentate gyrus (DG).We found that CX(3)CR1 deficiency increases hippocampal plasticity and spatial memory, blunting the potentiating effects of EE.These data indicate that CX(3)CL1/CX(3)CR1-mediated signaling is crucial for a normal experience-dependent modulation of hippocampal functions.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology and Pharmacology, Istituto Pasteur Fondazione Cenci Bolognetti, Università di Roma Rome Italy.

ABSTRACT
In recent years several evidence demonstrated that some features of hippocampal biology, like neurogenesis, synaptic transmission, learning, and memory performances are deeply modulated by social, motor, and sensorial experiences. Fractalkine/CX(3)CL1 is a transmembrane chemokine abundantly expressed in the brain by neurons, where it modulates glutamatergic transmission and long-term plasticity processes regulating the intercellular communication between glia and neurons, being its specific receptor CX(3)CR1 expressed by microglia. In this paper we investigated the role of CX(3)CL1/CX(3)CR1 signaling on experience-dependent hippocampal plasticity processes. At this aim wt and CX(3)CR1(GFP/GFP) mice were exposed to long-lasting-enriched environment (EE) and the effects on hippocampal functions were studied by electrophysiological recordings of long-term potentiation of synaptic activity, behavioral tests of learning and memory in the Morris water maze paradigm and analysis of neurogenesis in the subgranular zone of the dentate gyrus (DG). We found that CX(3)CR1 deficiency increases hippocampal plasticity and spatial memory, blunting the potentiating effects of EE. In contrast, exposure to EE increased the number and migration of neural progenitors in the DG of both wt and CX(3)CR1(GFP/GFP) mice. These data indicate that CX(3)CL1/CX(3)CR1-mediated signaling is crucial for a normal experience-dependent modulation of hippocampal functions.

No MeSH data available.


Related in: MedlinePlus