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Brain Structure and Function

, Volume 222, Issue 2, pp 1077–1085 | Cite as

Exposure to a diet high in fat attenuates dendritic spine density in the medial prefrontal cortex

  • Paige M. Dingess
  • Rebecca A. Darling
  • E. Kurt Dolence
  • Bruce W. Culver
  • Travis E. Brown
Short Communication

Abstract

A key factor in the development of obesity is the overconsumption of food calorically high in fat. Overconsumption of food high in fat not only promotes weight gain but elicits changes in reward processing. No studies to date have examined whether consumption of a high-fat (HF) diet alters structural plasticity in brain areas critical for reward processing, which may account for persistent changes in behavior and psychological function by reorganizing synaptic connectivity. To test whether dietary fat may induce structural plasticity we placed rats on one of three dietary conditions: ad libitum standard chow (SC), ad libitum 60 % HF (HF-AL), or calorically matched 60 % HF (HF-CM) for 3 weeks and then quantified dendritic spine density and type on basal and apical dendrites of pyramidal cells in layer V of the medial prefrontal cortex (mPFC) and medium spiny neurons (MSNs) of the nucleus accumbens. Our results demonstrate a significant reduction in the density of thin spines on the apical and basal segments of dendrites within the infralimbic, but not prelimbic, mPFC.

Keywords

High-fat Prefrontal cortex Plasticity Dendritic spines 

Notes

Acknowledgments

The authors would like to thank Dr. Zhaojie Zhang, the director of the Neuroscience microscopy facility at the University of Wyoming, for his help and guidance imaging the spine data. We would also like to thank Kevin Schlidt and Morgan Deters for their assistance with animal care. We are also grateful for the support contributed by NIGMS grant P30 GM103398, and the College of Health Sciences Seed Grant from the University of Wyoming.

References

  1. Vollbrecht PJ et al (2015) Pre-existing differences in motivation for food and sensitivity to cocaine-induced locomotion in obesity-prone rats. Physiol Behav 152(A):151–160Google Scholar
  2. Baldwin AE, Sadeghian K, Kelley AE (2002) Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J Neurosci 22(3):1063–1071PubMedGoogle Scholar
  3. Bechara A (2005) Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8(11):1458–1463CrossRefPubMedGoogle Scholar
  4. Bjorndal B et al (2011) Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes 2011:490650CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bloss EB et al (2011) Evidence for reduced experience-dependent dendritic spine plasticity in the aging prefrontal cortex. J Neurosci 31(21):7831–7839CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bray GA, Paeratakul S, Popkin BM (2004) Dietary fat and obesity: a review of animal, clinical and epidemiological studies. Physiol Behav 83(4):549–555CrossRefPubMedGoogle Scholar
  7. Calle EE (2007) Obesity and cancer. BMJ 335(7630):1107–1108CrossRefPubMedPubMedCentralGoogle Scholar
  8. Capriles N et al (2003) A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology 168(1–2):66–74CrossRefPubMedGoogle Scholar
  9. Cordeira JW et al (2010) Brain-derived neurotrophic factor regulates hedonic feeding by acting on the mesolimbic dopamine system. J Neurosci 30(7):2533–2541CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cornish JL, Duffy P, Kalivas PW (1999) A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior. Neuroscience 93(4):1359–1367CrossRefPubMedGoogle Scholar
  11. Crombag HS et al (2005) Opposite effects of amphetamine self-administration experience on dendritic spines in the medial and orbital prefrontal cortex. Cereb Cortex 15(3):341–348CrossRefPubMedGoogle Scholar
  12. Diana M, Spiga S, Acquas E (2006) Persistent and reversible morphine withdrawal-induced morphological changes in the nucleus accumbens. Ann NY Acad Sci 1074:446–457CrossRefPubMedGoogle Scholar
  13. Dong Y et al (2005) Cocaine-induced plasticity of intrinsic membrane properties in prefrontal cortex pyramidal neurons: adaptations in potassium currents. J Neurosci 25(4):936–940CrossRefPubMedGoogle Scholar
  14. Dumitriu D et al (2010) Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J Neurosci 30(22):7507–7515CrossRefPubMedPubMedCentralGoogle Scholar
  15. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399(6731):66–70CrossRefPubMedGoogle Scholar
  16. Ferrario CR et al (2005) Neural and behavioral plasticity associated with the transition from controlled to escalated cocaine use. Biol Psychiatry 58(9):751–759CrossRefPubMedGoogle Scholar
  17. Ferrario CR et al (2012) Withdrawal from cocaine self-administration alters NMDA receptor-mediated Ca2+ entry in nucleus accumbens dendritic spines. PLoS ONE 7(8):e40898CrossRefPubMedPubMedCentralGoogle Scholar
  18. Finkelstein EA et al (2009) Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff (Millwood) 28(5):w822–w831CrossRefGoogle Scholar
  19. Geiger BM et al (2008) Evidence for defective mesolimbic dopamine exocytosis in obesity-prone rats. FASEB J 22(8):2740–2746CrossRefPubMedPubMedCentralGoogle Scholar
  20. Geiger BM et al (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159(4):1193–1199CrossRefPubMedPubMedCentralGoogle Scholar
  21. Glantz LA, Lewis DA (2000) Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57(1):65–73CrossRefPubMedGoogle Scholar
  22. Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183(4675):1592–1593CrossRefPubMedGoogle Scholar
  23. Greenwood CE, Winocur G (1990) Learning and memory impairment in rats fed a high saturated fat diet. Behav Neural Biol 53(1):74–87CrossRefPubMedGoogle Scholar
  24. Hebebrand J, Hinney A (2009) Environmental and genetic risk factors in obesity. Child Adolesc Psychiatr Clin N Am 18(1):83–94CrossRefPubMedGoogle Scholar
  25. Hensrud DD (2004) Diet and obesity. Curr Opin Gastroenterol 20(2):119–124CrossRefPubMedGoogle Scholar
  26. Holtmaat A et al (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441(7096):979–983CrossRefPubMedGoogle Scholar
  27. Irwin SA, Galvez R, Greenough WT (2000) Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex 10(10):1038–1044CrossRefPubMedGoogle Scholar
  28. Johnson PM, Kenny PJ (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13(5):635–641CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162(8):1403–1413CrossRefPubMedGoogle Scholar
  30. Kleim JA et al (1996) Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci 16(14):4529–4535PubMedGoogle Scholar
  31. Kurth T et al (2002) Body mass index and the risk of stroke in men. Arch Intern Med 162(22):2557–2562CrossRefPubMedGoogle Scholar
  32. LaLumiere RT, Niehoff KE, Kalivas PW (2010) The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn Mem 17(4):168–175CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lee KW et al (2006) Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc Natl Acad Sci USA 103(9):3399–3404CrossRefPubMedPubMedCentralGoogle Scholar
  34. Masek J, Fabry P (1959) High-fat diet and the development of obesity in albino rats. Experientia 15:444–445CrossRefPubMedGoogle Scholar
  35. McFarland K, Kalivas PW (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 21(21):8655–8663PubMedGoogle Scholar
  36. McLaughlin J, See RE (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology 168(1–2):57–65CrossRefPubMedGoogle Scholar
  37. Muhammad A, Kolb B (2011) Maternal separation altered behavior and neuronal spine density without influencing amphetamine sensitization. Behav Brain Res 223(1):7–16CrossRefPubMedGoogle Scholar
  38. Nestler EJ (2005) The neurobiology of cocaine addiction. Sci Pract Perspect 3(1):4–10CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nicola SM, Surmeier J, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185–215CrossRefPubMedGoogle Scholar
  40. Oe Y et al (2013) Dendritic spine dynamics in synaptogenesis after repeated LTP inductions: dependence on pre-existing spine density. Sci Rep 3:1957CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ogden CL et al (2006) Prevalence of overweight and obesity in the United States, 1999–2004. JAMA 295(13):1549–1555CrossRefPubMedGoogle Scholar
  42. O’Malley A et al (2000) Transient spine density increases in the mid-molecular layer of hippocampal dentate gyrus accompany consolidation of a spatial learning task in the rodent. Neuroscience 99(2):229–232CrossRefPubMedGoogle Scholar
  43. Peters J, LaLumiere RT, Kalivas PW (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J Neurosci 28(23):6046–6053CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rasakham K et al (2014) Synapse density and dendritic complexity are reduced in the prefrontal cortex following 7 days of forced abstinence from cocaine self-administration. PLoS One 9(7):e102524CrossRefPubMedPubMedCentralGoogle Scholar
  45. Robinson TE, Kolb B (1999) Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur J Neurosci 11(5):1598–1604CrossRefPubMedGoogle Scholar
  46. Robinson MJ et al (2015) Individual differences in cue-induced motivation and striatal systems in rats susceptible to diet-induced obesity. Neuropsychopharmacology 40(9):2113–2123CrossRefPubMedPubMedCentralGoogle Scholar
  47. Schemmel R, Mickelsen O, Gill JL (1970) Dietary obesity in rats: body weight and body fat accretion in seven strains of rats. J Nutr 100(9):1041–1048PubMedGoogle Scholar
  48. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36(2):241–263CrossRefPubMedGoogle Scholar
  49. Shigeta H et al (2001) Lifestyle, obesity, and insulin resistance. Diabetes Care 24(3):608CrossRefPubMedGoogle Scholar
  50. Sobal J, Stunkard AJ (1989) Socioeconomic status and obesity: a review of the literature. Psychol Bull 105(2):260–275CrossRefPubMedGoogle Scholar
  51. Spence D (2011) Inactivity and obesity. BMJ 343:d5093CrossRefPubMedGoogle Scholar
  52. Tominaga-Yoshino K et al (2002) Repetitive activation of protein kinase A induces slow and persistent potentiation associated with synaptogenesis in cultured hippocampus. Neurosci Res 44(4):357–367CrossRefPubMedGoogle Scholar
  53. Tominaga-Yoshino K et al (2008) Repetitive induction of late-phase LTP produces long-lasting synaptic enhancement accompanied by synaptogenesis in cultured hippocampal slices. Hippocampus 18(3):281–293CrossRefPubMedGoogle Scholar
  54. Tseng KY, O’Donnell P (2004) Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 24(22):5131–5139CrossRefPubMedGoogle Scholar
  55. Volkow ND et al (2008a) Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci 363(1507):3191–3200CrossRefPubMedPubMedCentralGoogle Scholar
  56. Volkow ND et al (2008b) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. Neuroimage 42(4):1537–1543CrossRefPubMedPubMedCentralGoogle Scholar
  57. Wang GJ et al (2001) Brain dopamine and obesity. Lancet 357(9253):354–357CrossRefPubMedGoogle Scholar
  58. Wild SH, Byrne CD (2006) ABC of obesity. risk factors for diabetes and coronary heart disease. BMJ 333(7576):1009–1011CrossRefPubMedPubMedCentralGoogle Scholar
  59. Yamada Y et al (2006) Genetic factors for obesity. Int J Mol Med 18(5):843–851PubMedGoogle Scholar
  60. Yogev Y, Catalano PM (2009) Pregnancy and obesity. Obstet Gynecol Clin North Am 36(2):285–300Google Scholar
  61. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44(5):749–757CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Paige M. Dingess
    • 2
  • Rebecca A. Darling
    • 2
  • E. Kurt Dolence
    • 1
  • Bruce W. Culver
    • 1
  • Travis E. Brown
    • 1
    • 2
  1. 1.School of PharmacyUniversity of WyomingLaramieUSA
  2. 2.Neuroscience ProgramUniversity of WyomingLaramieUSA

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