Sex Differences in Long-Term Potentiation at Temporoammonic-CA1 Synapses: Potential Implications for Memory Consolidation

Qi, Xiaoqiang; Zhang, Ke; Xu, Ting; Yamaki, Vítor Nagai; Wei, Zhisheng; Huang, Mingfa; Rose, Gregory M.; Cai, Xiang

doi:10.1371/journal.pone.0165891

Cited by 48 publications

(42 citation statements)

References 74 publications

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“…A total of 180 transverse acute hippocampal slices (400 µm thick) from 100 adult male Wistar rats (5–7 weeks old) and 30 transverse acute hippocampal slices (400 µm thick) from three aged male mice (C57BL/6J, 16–18 months old) were used for electrophysiological experiments. We avoided using female rats and mice for our experiments primarily because hormonal alterations during the oestrous cycle can affect synaptic plasticity measurements (Monfort, Gomez‐Gimenez, Llansola, & Felipo, ; Qi et al, ; Warren, Humphreys, Juraska, & Greenough, ). Animals were housed under 12h light/12h dark conditions with food and water available ad libitum.…”

Section: Methodsmentioning

confidence: 99%

MicroRNA‐134‐5p inhibition rescues long‐term plasticity and synaptic tagging/capture in an Aβ(1–42)‐induced model of Alzheimer’s disease

et al. 2019

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Progressive memory loss is one of the most common characteristics of Alzheimer's disease (AD), which has been shown to be caused by several factors including accumulation of amyloid β peptide (Aβ) plaques and neurofibrillary tangles. Synaptic plasticity and associative plasticity, the cellular basis of memory, are impaired in AD.Recent studies suggest a functional relevance of microRNAs (miRNAs) in regulating plasticity changes in AD, as their differential expressions were reported in many AD brain regions. However, the specific role of these miRNAs in AD has not been elucidated. We have reported earlier that late long-term potentiation (late LTP) and its associative mechanisms such as synaptic tagging and capture (STC) were impaired in Aβ (1-42)-induced AD condition. This study demonstrates that expression of miR-134-5p, a brain-specific miRNA is upregulated in Aβ (1-42)-treated AD hippocampus.Interestingly, the loss of function of miR-134-5p restored late LTP and STC in AD.In AD brains, inhibition of miR-134-5p elevated the expression of plasticity-related proteins (PRPs), cAMP-response-element binding protein (CREB-1) and brain-derived neurotrophic factor (BDNF), which are otherwise downregulated in AD condition.The results provide the first evidence that the miR-134-mediated post-transcriptional regulation of CREB-1 and BDNF is an important molecular mechanism underlying the plasticity deficit in AD; thus demonstrating the critical role of miR-134-5p as a potential therapeutic target for restoring plasticity in AD condition.

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Section: Methodsmentioning

confidence: 99%

MicroRNA‐134‐5p inhibition rescues long‐term plasticity and synaptic tagging/capture in an Aβ(1–42)‐induced model of Alzheimer’s disease

et al. 2019

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“…Some studies reported overall superior spatial memory in WT male compared to female rodents (Monfort et al, 2015); others observed sex differences in search strategies, but not performance in spatial memory tasks (Locklear and Kritzer, 2014). Additional studies have reported sex differences only in spatial memory retention but not in short-term memory (Qi et al, 2016) or have found no spatial memory differences due to sex in WT young adult rodents (Frick et al, 1999;Dachtler et al, 2011). We did not observe differences in spatial memory in the Barnes maze between WT male and female 8 -12-week-old mice.…”

Section: Discussionmentioning

confidence: 99%

“…Multiple studies have also shown a sex-specific component in AMPAR-mediated synaptic plasticity underlying memory. Several studies have reported that differences between male and female rats in evoked AMPAR/NMDAR signaling in hippocampal synapses, along with differences in the magnitude of evoked LTP, may underlie sex differences in spatial memory (Monfort et al, 2015;Qi et al, 2016). Estrous has been shown to modulate diffusion of AMPARs to the surface in female mice (Palomero-Gallagher et al, 2003;Tada et al, 2015;Bechard et al, 2018), which may underlie part of the reported importance of estrogenic mechanisms for memory in females (Cordeira et al, 2018;Frick et al, 2018;Koss et al, 2018;Wang et al, 2018;Koebele et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Cornichon Homolog-3 (CNIH3) Modulates Spatial Memory in Female Mice

Frye

Williams

Trousdale

et al. 2019

Preprint

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Cornichon homolog-3 (CNIH3) is an AMPA receptor (AMPAR) auxiliary protein that traffics AMPARs to the postsynaptic membrane and potentiates AMPAR signaling. AMPARs are key components of hippocampal synaptic plasticity and memory formation, however the role of CNIH3 in memory has yet to be elucidated. To study the role of CNIH3 on mouse behavior, we bred and characterized a line of Cnih3 -/mice from C57BL/6 Cnih3 tm1a(KOMP)Wtsi mice obtained from the Knockout Mouse Project (KOMP). In agreement with previous studies of CNIH3 in the brain, we observed concentrated expression of Cnih3 in the dorsal hippocampus, a region associated with spatial learning and memory. Therefore, we tested Cnih3 +/+ , Cnih3 +/-, and Cnih3 -/mice in the Barnes maze paradigm to measure spatial memory. We observed no change in spatial memory in male Cnih3 +/and Cnih3 -/mice compared to male Cnih3 +/+ controls, however, Cnih3 -/female mice made significantly more primary errors, had a higher primary latency, and took less efficient routes to the target in the maze compared to Cnih3 +/+ female mice. Next, to investigate an enhancement of spatial memory by Cnih3 overexpression, specifically in the dorsal hippocampus, we developed an AAV5 viral construct to express wild-type Cnih3 in excitatory neurons. Female mice overexpressing Cnih3 made significantly fewer errors, had a lower primary latency to the target, and took more efficient routes to the maze target compared to YFP expressing control females. No change in spatial memory was observed in male Cnih3 overexpression mice. This study, the first to identify sex-specific effects of the AMPAR auxiliary protein CNIH3 on spatial memory, provides the groundwork for future studies investigating the role of CNIH3 on sexually dimorphic AMPAR-dependent behavior and hippocampal synaptic plasticity.

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“…In rodents, the eCB system sexual differences appear early in development (Craft et al, 2013). Sexually dimorphic regulation of synaptic plasticity or intrinsic neuronal activity in the amygdala (Bender et al, 2017; Chen et al, 2014; Fendt et al, 2013), hippocampus (Qi et al, 2016; Harte-Hargrove et al, 2015; Inoue et al, 2014; Huang and Woolley, 2012) and PFC (Li et al, 2016; Nakajima et al, 2014) have been described, but the effects of exogenous cannabinoids on synaptic plasticity in females as well as putative sex differences in its expression remain poorly explored. Our results showed that while eCB-LTD was not affected by cannabinoid exposure in pubescent and adult males, females’ eCB-LTD was ablated.…”

Section: Discussionmentioning

confidence: 99%

Sex differences in the behavioral and synaptic consequences of a single exposure to cannabinoid at puberty and adulthood

Borsoi

Manduca

Bara

et al. 2018

Preprint

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2Heavy cannabis consumption among adolescents is associated with significant and lasting 2 3 neurobiological, psychological and health consequences that depend on the age of first use. 4Chronic exposure to cannabinoid (CB) agonists during adolescence alters social behavior and 2 5 prefrontal cortex (PFC) activity in adult rats. However, sex differences on social behavior as 2 6well as PFC synaptic plasticity after acute CB activation remain poorly explored. Here, we 2 7 determined the consequences of a single CB activation differently affects PFC in males and 2 8 females by assessing social behavior and PFC neuronal and synaptic functions in rats during 2 9 pubertal or adulthood periods, 24h after a single in-vivo cannabinoid exposure (SCE). During 3 0 puberty, SCE reduced play behavior in females but not males. In contrast, SCE impaired 3 1 sociability in both sexes at adulthood. General exploration and memory recognition remained 3 2 normal at both ages and both sexes. At the synaptic level, SCE ablated endocannabinoid-3 3 mediated long-term depression (eCB-LTD) in the PFC of females of both ages and 3 4 heightened excitability of PFC pyramidal neurons at adulthood, while males were spared. In 3 5 contrast, SCE was associated to impaired long-term potentiation in adult males. Together, the 3 6 data indicate behavioral and synaptic sex differences in response to a single in-vivo exposure 3 7to cannabinoid at puberty and adulthood. 3 8 3 9

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Sex Differences in Long-Term Potentiation at Temporoammonic-CA1 Synapses: Potential Implications for Memory Consolidation

Cited by 48 publications

References 74 publications

MicroRNA‐134‐5p inhibition rescues long‐term plasticity and synaptic tagging/capture in an Aβ(1–42)‐induced model of Alzheimer’s disease

MicroRNA‐134‐5p inhibition rescues long‐term plasticity and synaptic tagging/capture in an Aβ(1–42)‐induced model of Alzheimer’s disease

Cornichon Homolog-3 (CNIH3) Modulates Spatial Memory in Female Mice

Sex differences in the behavioral and synaptic consequences of a single exposure to cannabinoid at puberty and adulthood

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