Chemogenetic silencing of hippocampus and amygdala reveals a double dissociation in periadolescent obesogenic diet-induced memory alterations

Naneix, Fabien; Bakoyiannis, Ioannis; Santoyo-Zedillo, Marianela; Bosch‐Bouju, Clémentine; Pacheco-López, Gustavo; Coutureau, Étienne

doi:10.1016/j.nlm.2020.107354

Cited by 11 publications

(13 citation statements)

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“…Our results indicate that periadolescent HFD induces long-term ORM deficits, corroborating our recent studies showing specific HFD effects on long-term, but not short-term, ORM (Biyong et al, 2021; Naneix et al, 2021). We had previously reported that chemogenetic inactivation of vHPC projecting neurons during training, by restricting DREADDs expression primarily to excitatory principal neurons thanks to the use of a CaMKII promoter, is able to restore HFD-induced ORM deficits 27 .…”

Section: Discussionsupporting

confidence: 92%

“…As chemogenetic vHPC silencing during ORM training restored HFD-induced long-term memory deficits (Naneix et al, 2021), we wondered to which extent the specific silencing of either NAc- or PFC-projecting vHPC cells upon CNO injection 45min before training could rescue these deficits (Figure 3A). Four groups were used for this purpose: CD, HFD control, HFD vHPC-NAc and HFD vHPC-mPFC (8-12 mice/group; see Table 3 for objects exploration during training and test).…”

Section: Resultsmentioning

confidence: 99%

“…Both surgeries and behavioural experiments were performed at adulthood. The day before euthanasia, fat mass (in grams) was measured by nuclear magnetic resonance (minispec LF90 II, Bruker, Wissembourg, 67166) (Naneix et al, 2021) and divided by body weight (in grams) as a ratio for each mouse. Three homozygous Ai14 Cre reporter adult mice [B6.Cg-Gt(ROSA) 26Sortm14(CAG-tdTomato)Hze /J or simply Ai14(RCL-tdT)-D; Jackson laboratory] under CD were also used to characterize vHPC-to-Nac and vHPC-to-mPFC pathways allowing the Cre-dependent expression of the red fluorophore td-Tomato specifically in vHPC projecting neurons and their efferents (see below).…”

Section: Methodsmentioning

confidence: 99%

“…We recently showed that object-based memory is impaired in HFD-exposed animals and that silencing of the ventral HPC (vHPC) with Designer Receptor Exclusively Activated by Designer Drugs (DREADD) rescued this memory deficits (Naneix et al, 2021). We therefore hypothesized that impairments in distinct components of object-based memory, namely recognition and location, in HFD animals could result from alterations of distinct vHPC efferent pathways.…”

Section: Introductionmentioning

confidence: 99%

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Obesogenic diet induces circuit-specific memory deficits in mice

Bakoyiannis

Ducourneau

N'diaye

et al. 2022

Preprint

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Obesity is associated with neurocognitive dysfunction, including memory deficits. This is particularly worrisome during adolescence, which represents a crucial period for maturation of brain structures, such as the hippocampus which are crucial for cognition. In rodent models, we recently reported that memory impairments induced by obesogenic high-fat diet (HFD) intake during the periadolescent period can be reversed by chemogenetic manipulation of the ventral hippocampus (vHPC). Here, we used an intersectional viral approach in HFD-fed male mice to chemogenetically inactivate specific vHPC efferent pathways to nucleus accumbens or medial prefrontal cortex during memory tasks. We first confirmed that HFD enhanced activation of both pathways after training and that our chemogenetic approach was effective in normalising this activation. Inactivation of the vHPC-nucleus accumbens pathway rescued HFD-induced deficits in recognition but not location memory. Conversely, inactivation of the vHPC-medial prefrontal cortex pathway restored location but not recognition memory impairments produced by HFD. Either pathway manipulation did not affect exploration, locomotion or anxiety-like behaviour. These findings suggest that HFD intake throughout adolescence impairs different types of memory through overactivation of specific hippocampal efferent pathways and that targeting these overactive pathways has therapeutic potential.

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Section: Discussionsupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Obesogenic diet induces circuit-specific memory deficits in mice

Bakoyiannis

Ducourneau

N'diaye

et al. 2022

Preprint

Self Cite

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“…Previous studies revealed that high-fat diet increased hippocampus IL-6 concentrations significantly when compared to normal diet (Dutheil et al, 2016, Farhangi et al, 2017. Additionally, Naneix et al (2021) showed the important role of hippocampus in high-fat diet-induced recognition memory impairment.…”

Section: Discussionmentioning

confidence: 98%

Effects of Indian Gooseberry Fruit on Anxiety-Related Behaviors and Memory Performance in High-fat Diet-induced Obese Mice

Juntapremjit¹,

Janthakhin²

2021

CMUJNS

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Indian gooseberry (Phyllanthus emblica L.) is widely used in Ayurvedic medicine, traditional Chinese medicine, as well as traditional medicine to treat health complications including disorders of diabetes and obesity. The aim of this study was to investigate the effects of Indian gooseberry fruit on anxiety-related behaviors and memory performance in high-fat diet-induced obese mice. C57BL/6 mice were randomly divided into four groups (n = 11 pre group); group 1: normal diet control, 2: normal diet treated with Indian gooseberry fruit juice, 3: high-fat diet control, and 4: high-fat diet treated with Indian gooseberry fruit juice. Each mouse was orally and daily administrated with 5mL/kg of Indian gooseberry fruit juice. After six weeks, all groups were tested for blood glucose levels, anxiety and memory performances, and the level of interleukin 6 (IL-6) in the hippocampus. The results revealed that the treatment with Indian gooseberry juice for six weeks produced a significant decrease in blood glucose levels (P <0.05). In anxiety-related behaviors, Indian gooseberry juice showed a remarkable decrease in self-grooming behavior (P <0.001). In addition, there was a significant increase in memory performance in the high-fat diet treated with Indian gooseberry fruit juice compared to the high-fat diet control (P <0.05). Furthermore, the level of inflammatory cytokine IL-6 in the hippocampus was significantly decreased after oral administration of Indian gooseberry fruit juice (P <0.05). These findings suggest that Indian gooseberry fruit can serve as a natural nutritional treatment for preventing high-fat diet-induced cognitive impairment. Keywords: Anxiety-related behaviors, High-fat diet, Indian gooseberry, Memory performance, Obesity

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Early‐life and chronic exposure to high‐fat diet alters noradrenergic and glutamatergic neurotransmission in the male rat amygdala and hippocampus under cognitive challenges

Osorio‐Gómez,

Perez,

Salcedo‐Tello

et al. 2024

J of Neuroscience Research

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Childhood obesity increases the risk of health and cognitive disorders in adulthood. Consuming high‐fat diets (HFD) during critical neurodevelopmental periods, like childhood, impairs cognition and memory in humans and animals, affecting the function and connectivity of brain structures related to emotional memory. However, the underlying mechanisms of such phenomena need to be better understood. This study aimed to investigate the neurochemical profile of the amygdala and hippocampus, brain structures involved in emotional memory, during the acquisition of conditioned odor aversion in male rats that consumed a HFD from weaning to adulthood. The rats gained weight, experienced metabolic changes, and reduced insulin sensitivity and glucose tolerance. Rats showed enhanced odor aversion memory, contrary to the expected cognitive impairments. This memory enhancement was accompanied by increased noradrenergic and glutamatergic neurotransmission in the amygdala and hippocampus. Importantly, this upregulation was specific to stimuli exposure, as basal neurotransmitter levels remained unaltered by the HFD. Our results suggest that HFD modifies cognitive function by altering neurochemical signaling, in this case, upregulating neurotransmitter levels rendering a stronger memory trace, demonstrating that metabolic dysfunctions do not only trigger exclusively detrimental plasticity processes but also render enhanced plastic effects depending on the type of information.

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Chemogenetic silencing of hippocampus and amygdala reveals a double dissociation in periadolescent obesogenic diet-induced memory alterations

Cited by 11 publications

References 100 publications

Obesogenic diet induces circuit-specific memory deficits in mice

Obesogenic diet induces circuit-specific memory deficits in mice

Effects of Indian Gooseberry Fruit on Anxiety-Related Behaviors and Memory Performance in High-fat Diet-induced Obese Mice

Early‐life and chronic exposure to high‐fat diet alters noradrenergic and glutamatergic neurotransmission in the male rat amygdala and hippocampus under cognitive challenges

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