Consumption of a High-Fat Diet Alters Perineuronal Nets in the Prefrontal Cortex.

P M Dingess,Z Zhang,T E Brown,S S Wulff,B A Sorg,J H Harkness,M Slaker

doi:10.1155/2018/2108373

Abstract

A key factor in the development of obesity is the overconsumption of fatty foods, which, in addition to facilitating weight gain, alters neuronal structures within brain reward circuitry. Our previous work demonstrates that sustained consumption of a high-fat diet (HFD) attenuates spine density in the prefrontal cortex (PFC). Whether HFD promotes structural adaptation among inhibitory cells of the PFC is presently unknown. One structure of interest is the perineuronal net (PNN), a specialized extracellular matrix surrounding, primarily, parvalbumin-containing GABAergic interneurons. PNNs contribute to synaptic stabilization, protect against oxidative stress, regulate the ionic microenvironment within cells, and modulate regional excitatory output. To examine diet-induced changes in PNNs, we maintained rats on one of three dietary conditions for 21 days: ad libitum chow, ad libitum 60% high fat (HF-AL), or limited-access calorically matched high fat (HF-CM), which produced no significant change in weight gain or adiposity with respect to chow controls. The PNN “number” and intensity were then quantified in the prelimbic (PL-PFC), infralimbic (IL-PFC), and ventral orbitofrontal cortex (OFC) using Wisteria floribunda agglutinin (WFA). Our results demonstrated that fat exposure, independent of weight gain, induced a robust decrease in the PNN intensity in the PL-PFC and OFC and a decrease in the PNN number in the OFC.

Highlights

While there are many behavioral, environmental, and even genetic circumstances that contribute to the development of obesity [1], the overconsumption of fatty foods is a major catalyst [2, 3]
Our previous work, demonstrating that rats fed with a HF diet exhibit an attenuation of spine density on pyramidal neurons of the infralimbic prefrontal cortex (IL-PFC) [10], suggests that the PFC may be a critical target of dietinduced structural change
Our results show for the first time that dietary fat alters perineuronal net (PNN) in the PFC, most robustly in the prelimbic PFC (PL-PFC) and orbitofrontal cortex (OFC) subregions

Summary

Introduction

While there are many behavioral, environmental, and even genetic circumstances that contribute to the development of obesity [1], the overconsumption of fatty foods is a major catalyst [2, 3]. Studies demonstrate that demographic factors such as age and gender influence poor adherence to diet and exercise regimens, but that poor adherence is especially prevalent among individuals who are already overweight or obese [5, 6]. This raises an interesting question—does the consumption of HF food induce changes in reward circuit neurophysiology that impair an individual’s ability to make favorable decisions regarding their health?. Our previous work, demonstrating that rats fed with a HF diet exhibit an attenuation of spine density on pyramidal neurons of the infralimbic prefrontal cortex (IL-PFC) [10], suggests that the PFC may be a critical target of dietinduced structural change

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Conclusion