Altered Odor-Induced Brain Activity as an Early Manifestation of Cognitive Decline in Patients With Type 2 Diabetes

Zhang, Zhou; Zhang, Bing; Wang, Xin; Zhang, Xin; Yang, Qing; Qing, Zhao; Lu, Jiaming; Bi, Yan; Zhu, Dalong

doi:10.2337/db17-1274

Cited by 39 publications

(55 citation statements)

References 47 publications

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“… 6 − 9 Furthermore, olfactory dysfunctions in type 2 diabetes (T2D) are strongly associated with cognitive impairment, 10 and T2D can induce early alterations in the olfactory system preceding cognitive decline. 11 Overall, these data suggest that olfactory deficits in T2D could represent an early marker of cognitive decline.…”

Section: Introductionmentioning

confidence: 81%

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Lietzau

Nyström

Wang

et al. 2020

ACS Chem. Neurosci.

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Olfactory dysfunction could be an early indicator of cognitive decline in type 2 diabetes (T2D). However, whether obesity affects olfaction in people with T2D is unclear. This question needs to be addressed, because most people with T2D are obese. Importantly, whether different contributing factors leading to obesity (e.g., different components of diet or gain in weight) affect specific olfactory functions and underlying mechanisms is unknown. We examined whether two T2D-inducing obesogenic diets, one containing a high proportion of fat (HFD) and one with moderate fat and high sugar (Western diet, WD), affect odor detection/discrimination, odor-related learning, and olfactory memory in the mouse. We also investigated whether the diets impair adult neurogenesis, GABAergic interneurons, and neuroblasts in the olfactory system. Here, we further assessed olfactory cortex volume and cFos expression-based neuronal activity. The WD-fed mice showed declined odor-related learning and olfactory memory already after 3 months of diet intake ( p = 0.046), although both diets induced similar hyperglycemia and weight gain compared to those of standard diet-fed mice ( p = 0.0001 and p < 0.0001, respectively) at this time point. Eight months of HFD and WD diminished odor detection ( p = 0.016 and p = 0.045, respectively), odor-related learning ( p = 0.015 and p = 0.049, respectively), and olfactory memory. We observed no changes in the investigated cellular mechanisms. We show that the early deterioration of olfactory parameters related to learning and memory is associated with a high content of sugar in the diet rather than with hyperglycemia or weight gain. This finding could be exploited for understanding, and potentially preventing, cognitive decline/dementia in people with T2D. The mechanisms behind this finding remain to be elucidated.

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Section: Introductionmentioning

confidence: 81%

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Lietzau

Nyström

Wang

et al. 2020

ACS Chem. Neurosci.

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“…Given that smell modulates taste perception to influence food intake, more neuroimaging studies of smell in obesity are also needed. Indeed, application of odorant stimuli delivery techniques to neuroimaging procedures such as fMRI and EEG has started to gain traction in recent years [ 152 , 153 ]. Further neuroimaging research is also needed to better characterize the influence that taste receptors in the gut have on brain responses following food consumption.…”

Section: Discussionmentioning

confidence: 99%

Brain Imaging of Taste Perception in Obesity: a Review

et al. 2019

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Purpose of Review We summarize neuroimaging findings related to processing of taste (fat, salt, umami, bitter, and sour) in the brain and how they influence hedonic responses and eating behaviors and their role in obesity. Recent Findings Neuroimaging studies in obese individuals have revealed alterations in reward/motivation, executive control/ self-regulation, and limbic/affective circuits that are implicated in food and drug addiction. Psychophysical studies show that sensory properties of food ingredients may be associated with anthropometric and neurocognitive outcomes in obesity. However, few studies have examined the neural correlates of taste and processing of calories and nutrient content in obesity. Summary The literature of neural correlated of bitter, sour, and salty tastes remains sparse in obesity. Most published studies have focused on sweet, followed by fat and umami taste. Studies on calorie processing and its conditioning by preceding taste sensations have started to delineate a dynamic pattern of brain activation associated with appetition. Our expanded understanding of taste processing in the brain from neuroimaging studies is poised to reveal novel prevention and treatment targets to help address overeating and obesity.

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“…Control subjects without diabetes received a standard 75‐g oral glucose tolerance test (OGTT) to ensure normal glucose tolerance, whereas participants with type 2 diabetes underwent a standard 100‐g steamed‐bread meal tolerance test, as previously described . The streamed bread was made of quantitative 100‐g flour which contained 75‐g carbohydrates.…”

Section: Methodsmentioning

confidence: 99%

“…6 Control subjects without diabetes received a standard 75-g oral glucose tolerance test (OGTT) to ensure normal glucose tolerance, whereas participants with type 2 diabetes underwent a standard 100-g steamed-bread meal tolerance test, as previously described. 14 The streamed bread was made of quantitative 100-g flour which contained 75-g carbohydrates. Fasting blood samples of participants were collected after overnight fast for 8 hours, immediately followed by a standard 75-g OGTT or 100-g steamed-bread meal tolerance test, with serum samples obtained before and 120 minutes after oral glucose load to measure C-peptide.…”

Section: Methodsmentioning

confidence: 99%

Improved skeletal muscle energy metabolism relates to the recovery of β cell function by intensive insulin therapy in drug naïve type 2 diabetes

Tang

Zhang

Wang

et al. 2019

Diabetes Metabolism Res

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Aims Diminished energy turnover of skeletal muscle is involved in the development of type 2 diabetes. Intensive insulin therapy has been reported to maintain glycaemic control in newly diagnosed type 2 diabetes, while the underlying mechanism remains unclear. Herein, we aimed to characterize the contribution of muscular mitochondrial oxidative phosphorylation (OxPhos) activity to insulin‐induced glycaemic control. Materials and methods There were 21 drug naïve patients with type 2 diabetes receiving continuous subcutaneous insulin infusion for 7 days. Nine nondiabetics matched for age, body mass index, and physical activity were recruited as controls. We applied 31P magnetic resonance spectroscopy to record in vivo muscular phosphocreatine (PCr) flux in controls and diabetics before and after insulin therapy. The mitochondrial OxPhos rate was calculated as ΔPCr / Δtime during the first 50 seconds after cessation of exercise. Results In drug naïve type 2 diabetes, muscular mitochondrial OxPhos rate was restored after insulin therapy. Notably, this alteration was positively associated with the improvements of 1,5‐anhydroglucitol, a serum marker for glucose control over the last 1 week, as well as homeostasis model assessment of β cell function and C‐peptide/glucose ratio t0, two indices for basal insulin secretion. Furthermore, patients with diabetes family history and more severe glucotoxicity tend to achieve greater improvement in mitochondrial function by insulin. Conclusions This study provides evidence that intensive insulin therapy facilitates muscular energy metabolism in drug naïve type 2 diabetes. It correlates to the recovery of β cell function, contributing to insulin‐induced glucose control.

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Altered Odor-Induced Brain Activity as an Early Manifestation of Cognitive Decline in Patients With Type 2 Diabetes

Cited by 39 publications

References 47 publications

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Western Diet Accelerates the Impairment of Odor-Related Learning and Olfactory Memory in the Mouse

Brain Imaging of Taste Perception in Obesity: a Review

Improved skeletal muscle energy metabolism relates to the recovery of β cell function by intensive insulin therapy in drug naïve type 2 diabetes

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