A high-fat diet decreases GABA concentration in the frontal cortex and hippocampus of rats

Cuauhtemoc Sandoval-Salazar, Joel Ramírez-Emiliano, Aurora Trejo-Bahena, Cecilia I Oviedo-Solís, Martha Silvia Solís-Ortiz, Cuauhtemoc Sandoval-Salazar, Joel Ramírez-Emiliano, Aurora Trejo-Bahena, Cecilia I Oviedo-Solís, Martha Silvia Solís-Ortiz

Abstract

Background: It has been proposed that the γ-aminobutyric acid (GABA) plays a key role in the regulation of food intake and body weight by controlling the excitability, plasticity and the synchronization of neuronal activity in the frontal cortex (FC). It has been also proposed that the high-fat diet (HFD) could disturb the metabolism of glutamate and consequently the GABA levels, but the mechanism is not yet clearly understood. Therefore, the aim of this study was to investigate the effect of a HFD on the GABA levels in the FC and hippocampus of rats.

Results: The HFD significantly increased weight gain and blood glucose levels, whereas decreased the GABA levels in the FC and hippocampus compared with standard diet-fed rats.

Conclusions: HFD decreases GABA levels in the FC and hippocampus of rat, which likely disrupts the GABAergic inhibitory processes, underlying feeding behavior.

Figures

Fig. 1
Fig. 1
Effect of high-fat diet on body weight gain. SD, standard diet (n = 10); HFD, high-fat diet (n = 10). Data are given as the mean ± standard error of the mean (SEM)
Fig. 2
Fig. 2
Effect of high-fat diet on GABA levels in frontal cortex and hippocampus. SD, standard diet (n = 10); HFD, high-fat diet (n = 10). Data are given as the mean ± standard error of the mean (SEM)

References

    1. Kaur J. A comprehensive review on metabolic syndrome. Cardiol Res Pract. 2014;2014:1–21.
    1. Okereke OI, Rosner B, Kim DH, Kang JH, Cook NR, Manson JE, Buring JE, Willett WC, Grodstein F. Dietary fat types and 4 year cognitive change in community-dwelling older women. Ann Neurol. 2013;72:124–134. doi: 10.1002/ana.23593.
    1. Panchal SK, Poudyal H, Iyer A, Nazer R, Alam MA, Diwan V, Kauter K, Sernia C, Campbell F, Ward L, Gobe G, Fenning A, Brown L. High-carbohydrate, high-fat diet-induced metabolic syndrome and cardiovascular remodeling in rats. J Cardiovasc Pharmacol. 2011;57:611–624. doi: 10.1097/FJC.0b013e3181feb90a.
    1. Farrar M, Font L, Pereira M, Mingote S, Bunce JG, Chrobak JJ, Salamone JD. Forebrain circuitry involved in effort-related choice: injections of the GABAA agonist muscimol into ventral pallidum alter response allocation in food-seeking behavior. Neuroscience. 2008;152:321–330. doi: 10.1016/j.neuroscience.2007.12.034.
    1. Owens DF, Kriegstein AR. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci. 2002;3:715–727. doi: 10.1038/nrn919.
    1. Avena NM, Bocarsly ME, Murray S, Gold MS. Effects of baclofen and naltrexone, alone and in combination, on the consumption of palatable food in male rats. Exp Clin Psychopharm. 2014;22:460–467. doi: 10.1037/a0037223.
    1. Page KA, Seo D, Belfort-DeAguiar R, Lacadie C, Dzuira J, Naik S, Amarnath S, Constable RT, Sherwin RS, Sinha R. Circulating glucose levels modulate neural control of desire for high-calorie food in humans. J Clin Inv. 2011;121:4161–4169. doi: 10.1172/JCI57873.
    1. Cohen J, Yates K, Duong M, Convit A. Obesity, orbitofrontal structure and function are associated with food choice: a cross-sectional study. BMJ Open. 2011;2:1–8.
    1. Ochner CN, Green D, Steenburgh JJ, Kounios J, Lowe MR. Asymemetric prefrontal cortex activation in relation to markers of overeating in obese humans. Appetite. 2010;53:44–49. doi: 10.1016/j.appet.2009.04.220.
    1. Alonso-Alonso M, Pascual-Leone A. The right brain hypothesis for obesity. JAMA. 2007;297:1819–1822. doi: 10.1001/jama.297.16.1819.
    1. Li M, Long C, Yang L. Hippocampal-prefrontal circuit and disrupted functional connectivity in psychiatric and neurodegenerative disorders. Biomed Res Int. 2015;2015:1–10.
    1. Kanoski SE, Hayes MR, Greenwald HS, Fortin SM, Gianessi CA, Gilbert JR, Grill HJ. Hippocampal leptin signaling reduces food intake and modulates food-related memory processing. Neuropsychopharmacology. 2011;36:1859–1870. doi: 10.1038/npp.2011.70.
    1. Valladolid-Acebes I, Merino B, Principato A, Fole A, Barbas C, Lorenzo MP, García A, Del Olmo N, Ruiz-gayo M, Cano V. High-fat diets induce changes in hippocampal glutamate metabolism and neurotransmission. Am J Physiol Endocrinol Metab. 2012;302:396–402. doi: 10.1152/ajpendo.00343.2011.
    1. Sickmann HM, Waagepetersen HS, Schousboe A, Benie AJ, Bouman SD. Obesity and type 2 diabetes in rats are associated with altered brain glycogen and amino-acid homeostasis. J Cereb Blood Flow Metab. 2010;30:1527–1537. doi: 10.1038/jcbfm.2010.61.
    1. Hao S, Dey A, Yu X, Stranahan AM. Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun. 2015;2015:1–10.
    1. Barry D, Clarke M, Petry NM. Obesity and its relationship to addictions: is overeating a form of addictive behavior? Am J Addict. 2010;18:439–451. doi: 10.3109/10550490903205579.
    1. Le Lay S, Simard G, Martinez MC, Andriantsitohaina R. Oxidative Stress and Metabolic Pathologies: from an Adipocentric Point of View. Oxid Med Cell Longev. 2014;2014:1–18. doi: 10.1155/2014/908539.
    1. Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol. 2010;9:367–377. doi: 10.1038/nrm2391.
    1. Vizioli C, Ghizoni DC, Rodrigues F, Gasparin S, Constantin P. Catabolism of amino acids in livers from cafeteria-fed rats. Mol Cell Biochem. 2013;373:265–277. doi: 10.1007/s11010-012-1499-0.
    1. Sweazea KL, Lekic M, Walker BR. Comparison of mechanisms involved in impaired vascular reactivity between high sucrose and high fat diets in rats. Nut Metabol. 2010;7:1–10. doi: 10.1186/1743-7075-7-1.
    1. Vecoli C, Novelli M, Pippa A, Giacopelli D, Beffy P, Masiello P, Abbate AL, Neglia D. Partial deletion of enos gene causes hyperinsulinemic state, unbalance of cardiac insulin signaling pathways and coronary dysfunction independently of high fat diet. PLoS One. 2014;9:1–11. doi: 10.1371/journal.pone.0104156.
    1. Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT, Newgard CB, Makowski L. Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity. 2011;19:1109–1117. doi: 10.1038/oby.2011.18.
    1. Brandt N, De Bock K, Richter EA, Hespel P. Cafeteria diet-induced insulin resistance is not associated with decreased insulin signaling or AMPK activity and is alleviated by physical training in rats. Am J Physiol Endocrinol Metab. 2010;299:215–224.
    1. Levin BE, Kang L, Sanders NM, Dunn-Meynell A. Role of neuronal glucosensing in the regulation of energy homeostasis. Diabetes. 2006;55:122–130. doi: 10.2337/db06-S016.
    1. Koopman KE, Booij J, Fliers E, Serlie MJ, la Fleur SE. Diet-induced changes in the lean brain: hypercaloric high-fat-high-sugar snacking decreases serotonin transporters in the human hypothalamic region. Mol Metab. 2013;2:417–422. doi: 10.1016/j.molmet.2013.07.006.
    1. Beleboni RO, Carolino RO, Pizzo AB, Castellan-Baldan L, Coutinho-Netto J, dos Santos WF, Coimbra NC. Pharmacological and biochemical aspects of GABAergic neurotransmission: pathological and neuropsychobiological relationships. Cell Mol Neurobiol. 2004;24:707–728. doi: 10.1007/s10571-004-6913-z.
    1. Newman S, Pascal L, Sadeghian K, Baldo BA. Sweetened-fat intake sensitizes gamma-aminobutyric acid mediated feeding responses elicited from the nucleus accumbens shell. Biol Psychiatry. 2014;73:1–18.
    1. Baldo B, Spencer RC, Sadeghian K, Mena JD. GABA-mediated inactivation of medial prefrontal and agranular insular cortex in the rat: contrasting effects on hunger- and palatability-driven feeding. Neuropsychopharmacol. 2015;41:960–970. doi: 10.1038/npp.2015.222.
    1. Le DS, Pannacciulli N, Chen K, Del Parigi A, Salbe AD, Reiman EM, Krakoff J. Less activation of the left dorsolateral prefrontal cortex in response to a meal: a feature of obesity. Am J Clin Nutr. 2006;84:725–731.
    1. Treviño S, Aguilar-Alonso P, Flores JA, Brambila E, Guevara J, Flores G, Lopez-Lopez G, Muñoz-Arenas G, Morales-Medina JC, Toxqui V, Venegas B, Diaz A. A high Calorie diet causes memory loss, metabolic syndrome and oxidative stress into hippocampus and temporal cortex of rats. Synapse. 2015;433:421–433. doi: 10.1002/syn.21832.
    1. Zhang B, Tian D, Yu C, Zhang J, Tian X, von Deneen K, Zang Y, Walter M, Liu Y. Altered baseline brain activities before food intake in obese men: a resting state fMRI study. Neurosci Lett. 2015;584:156–161. doi: 10.1016/j.neulet.2014.10.020.
    1. Kang X, Xiao J, Huang X, Gu Z. Optimization of dansyl derivatization and chromatographic conditions in the determination of neuroactive amino acids of biological samples. Clin Chim Acta. 2006;366:352–356. doi: 10.1016/j.cca.2005.11.011.

Source: PubMed

3
Tilaa