Western High-Fat Diet Consumption during Adolescence Increases Susceptibility to Traumatic Stress while Selectively Disrupting Hippocampal and Ventricular Volumes

Kalyan-Masih, Priya; Vega-Torres, Julio David; Miles, Christina; Haddad, Elizabeth; Rainsbury, Sabrina; Baghchechi, Mohsen; Obenaus, André; Figueroa, Johnny D.

doi:10.1523/eneuro.0125-16.2016

Cited by 54 publications

(75 citation statements)

References 129 publications

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“…Adolescent (ADOL: postnatal day, PND, 24) and adult (ADUL: PND 74) male Lewis rats were purchased from Charles River Laboratories (Portage, MI, USA). The rationale for the use of Lewis rats is based on the relevant vulnerabilities of this strain to post-traumatic stress (Kalyan-Masih et al, 2016;Vega-Torres et al, 2018). Immediately upon arrival, the rats were housed in groups (2 per cage) with free access to food and water.…”

Section: Animalsmentioning

confidence: 99%

“…Acoustic stimuli intensities and response sensitivities were calibrated before commencing the experiments. The ASR protocol has been previously described by our group (Kalyan-Masih et al, 2016;Vega-Torres et al, 2018). Briefly, experimental sessions were 22 min long and started with a 5-min habituation period (background noise = 60 decibels, dB).…”

Section: Acoustic Startle Reflex (Asr)mentioning

confidence: 99%

“…Enclosures were thoroughly cleaned and dried following each session. Averaged ASR magnitudes were normalized by weight to eliminate confounding factors associated with body weight (Weight-corrected ASR = maximum startle magnitude in mV divided by body weight at testing day) (Elkin et al, 2006;Gogos et al, 1999;Grimsley et al, 2015;Kalyan-Masih et al, 2016;Vega-Torres et al, 2018).…”

Section: Acoustic Startle Reflex (Asr)mentioning

confidence: 99%

“…Early-life trauma is linked to obesity and the consumption of obesogenic diets (Duncan et al, 2015;Ehlert, 2013;Farr et al, 2015;Masodkar et al, 2016;Mason et al, 2017;Pagoto et al, 2012;Perkonigg et al, 2009;Roenholt et al, 2012;Wolf et al, 2017). The high co-morbidity between obesity and post-traumatic stress disorders (PTSD) suggest that adaptations to trauma may increase the risk for the consumption of obesogenic diets as a result of the traumatic experience (Godfrey et al, 2018;Kalyan-Masih et al, 2016;Michopoulos et al, 2016). There is also mounting evidence that exposure to obesogenic diets rich in saturated fat foods and sugars have a direct adverse effect on emotional regulation, anxiety-like behaviors, and neural substrates implicated with stress (Baker and Reichelt, 2016;Boitard et al, 2015;Kalyan-Masih et al, 2016;Ortolani et al, 2011;Reichelt et al, 2015;Sivanathan et al, 2015;Vega-Torres et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…The high co-morbidity between obesity and post-traumatic stress disorders (PTSD) suggest that adaptations to trauma may increase the risk for the consumption of obesogenic diets as a result of the traumatic experience (Godfrey et al, 2018;Kalyan-Masih et al, 2016;Michopoulos et al, 2016). There is also mounting evidence that exposure to obesogenic diets rich in saturated fat foods and sugars have a direct adverse effect on emotional regulation, anxiety-like behaviors, and neural substrates implicated with stress (Baker and Reichelt, 2016;Boitard et al, 2015;Kalyan-Masih et al, 2016;Ortolani et al, 2011;Reichelt et al, 2015;Sivanathan et al, 2015;Vega-Torres et al, 2018). Therefore, early-life exposure to obesogenic diets may predispose individuals to maladaptive stress responses, resulting in increased PTSD risk.…”

Section: Introductionmentioning

confidence: 99%

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Early maturational emergence of adult-like emotional reactivity and anxiety after brief exposure to an obesogenic diet

Vega-Torres

Azadian

Rios-Orsini

et al. 2020

Preprint

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Background: Emerging evidence demonstrates that diet-induced obesity disrupts corticolimbic circuits underlying emotional regulation. Studies directed at understanding how obesity alters brain and behavior are easily confounded by a myriad of complications related to obesity. This study investigated the early neurobiological stress response triggered by an obesogenic diet. Furthermore, this study directly determined the combined impact of a short-term obesogenic diet and adolescence on critical behavioral and molecular substrates implicated in emotion regulation and stress.Methods: Adolescent (postnatal day 31) or adult (postnatal day 81) Lewis rats were fed for one week with an experimental Western-like high-saturated fat diet (WD, 41% kcal from fat) or a matched control diet (CD, 13% kcal from fat). We used the acoustic fear-potentiated startle (FPS) paradigm to determine the effects of the WD on cued fear conditioning and fear extinction. We used c-Fos mapping to determine the functional influence of the diet and stress on corticolimbic circuits. Results:We report that one-week WD consumption was sufficient to induce fear extinction deficits in adolescent rats, but not in adult rats. We identify fear-induced alterations in corticolimbic neuronal activation and demonstrate increased prefrontal cortex CRHR1 mRNA levels in the rats that consumed the WD. Conclusions:Our findings demonstrate that short-term consumption of an obesogenic diet during adolescence heightens behavioral and molecular vulnerabilities associated with risk for anxiety and stress-related disorders. Given that fear extinction promotes resilience, and that fear extinction principles are the Vega-Torres et. al., 3 foundation of psychological treatments for PTSD, understanding how obesogenic environments interact with the adolescent period to affect the acquisition and expression of fear extinction memories is of tremendous clinical relevance. KEYWORDS PTSD, diet-induced obesity, adolescence, anxiety, fear-potentiated startle, CRHR1 HIGHLIGHTS • Short-term WD consumption during adolescence impairs cued fear extinction memory retention in a fear-potentiated startle paradigm.• Short-term WD consumption during adolescence attenuates neuronal activation to electric footshock stress in the basomedial nuclei of the amygdala.• Short-term WD consumption increases CRHR1 mRNA levels in the medial prefrontal cortex.• Adult LEW rats exhibit increased basal HPA axis tone and heightened emotional reactivity to footshock stress relative to adolescent rats.

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Section: Animalsmentioning

confidence: 99%

Section: Acoustic Startle Reflex (Asr)mentioning

confidence: 99%

Section: Acoustic Startle Reflex (Asr)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Early maturational emergence of adult-like emotional reactivity and anxiety after brief exposure to an obesogenic diet

Vega-Torres

Azadian

Rios-Orsini

et al. 2020

Preprint

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Role of the prefrontal cortical protease TACE/ADAM17 in neurobehavioral responses to chronic stress during adolescence

Sharafeddin,

Sierra,

Ghaly

et al. 2024

Brain and Behavior

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IntroductionChronic adolescent stress profoundly affects prefrontal cortical networks regulating top‐down behavior control. However, the neurobiological pathways contributing to stress‐induced alterations in the brain and behavior remain largely unknown. Chronic stress influences brain growth factors and immune responses, which may, in turn, disrupt the maturation and function of prefrontal cortical networks. The tumor necrosis factor alpha‐converting enzyme/a disintegrin and metalloproteinase 17 (TACE/ADAM17) is a sheddase with essential functions in brain maturation, behavior, and inflammatory responses. This study aimed to determine the impact of stress on the prefrontal cortex and whether TACE/ADAM17 plays a role in these responses.MethodsWe used a Lewis rat model that incorporates critical elements of chronic psychosocial stress, such as uncontrollability, unpredictability, lack of social support, and re‐experiencing of trauma.ResultsChronic stress during adolescence reduced the acoustic startle reflex and social interactions while increasing extracellular free water content and TACE/ADAM17 mRNA levels in the medial prefrontal cortex. Chronic stress altered various ethological behavioral domains in the observation home cages (decreased ingestive behaviors and increased walking, grooming, and rearing behaviors). A group of rats was injected intracerebrally either with a novel Accell™ SMARTpool TACE/ADAM17 siRNA or a corresponding siRNA vehicle (control). The RNAscope Multiplex Fluorescent v2 Assay was used to visualize mRNA expression. Automated puncta quantification and analyses demonstrated that TACE/ADAM17 siRNA administration reduced TACE/ADAM17 mRNA levels in the medial prefrontal cortex (59% reduction relative to control). We found that the rats that received prefrontal cortical TACE/ADAM17 siRNA administration exhibited altered eating patterns (e.g., increased food intake and time in the feeding zone during the light cycle).ConclusionThis study supports that the prefrontal cortex is sensitive to adolescent chronic stress and suggests that TACE/ADAM17 may be involved in the brain responses to stress.

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The effect of body mass index on hippocampal morphology and memory performance in late childhood and adolescence

et al. 2020

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Childhood obesity is associated with negative physiological and cognitive health outcomes. The hippocampus is a diverse subcortical structure involved in learned feeding behaviors and energy regulation, and research has shown that the hippocampus is vulnerable to the effects of excess adiposity. Previous studies have demonstrated reduced hippocampal volume in overweight and obese children; however, it is unclear if certain subregions are selectively affected. The purpose of this study was to determine how excess body weight influences regional hippocampal surface morphology and memory performance in a large cross-sectional cohort of 588 children and adolescents between 8.33 and 19.92 years of age using body mass index expressed as a percentage of the 95th percentile cutoff (%BMIp95). We demonstrate %BMIp95 is associated with reduced radial thickness in the superior anterior region of the left hippocampus, and this relationship is predominantly driven by children younger than 14 years. We also found %BMIp95 was associated with worse performance on a spatial episodic memory task and this relationship was partially mediated by the radial thickness of the significant shape cluster. These results demonstrate the differential influence of excess body weight on regional hippocampal structure and hippocampal-dependent behavior in children and adolescents.

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Western High-Fat Diet Consumption during Adolescence Increases Susceptibility to Traumatic Stress while Selectively Disrupting Hippocampal and Ventricular Volumes

Cited by 54 publications

References 129 publications

Early maturational emergence of adult-like emotional reactivity and anxiety after brief exposure to an obesogenic diet

Early maturational emergence of adult-like emotional reactivity and anxiety after brief exposure to an obesogenic diet

Role of the prefrontal cortical protease TACE/ADAM17 in neurobehavioral responses to chronic stress during adolescence

The effect of body mass index on hippocampal morphology and memory performance in late childhood and adolescence

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