Obesity diminishes synaptic markers, alters Microglial morphology, and impairs cognitive function

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 51, 2015, Pages 15731-15736

  Bocarsly, Miriam E ^a   Fasolino, Maria ^a   Kane, Gary A ^a   Lamarca, Elizabeth A ^a   Kirschen, Gregory W ^a   Karatsoreos, Ilia N ^b,c   McEwen, Bruce S ^c   Gould, Elizabeth ^a  

^a PRINCETON UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Cognition; Dendritic spine; Microglia; Obesity; Prefrontal cortex

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL DENSITY; CELL STRUCTURE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC SPINE; DIABETES MELLITUS; DIET INDUCED OBESITY; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; METABOLIC SYNDROME X; MICROGLIA; NONHUMAN; PERIRHINAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SYNAPSE; WESTERN BLOTTING; ANIMAL; CELL SHAPE; CHEMISTRY; COGNITION DISORDERS; COMPLICATION; DENDRITE; DISEASE MODEL; OBESITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANXIETY; CELL SHAPE; COGNITION DISORDERS; DENDRITES; DISEASE MODELS, ANIMAL; MALE; MICROGLIA; OBESITY; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 84952684821     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1511593112     Document Type: Article

References (54)

1. Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 307(5):491-497.
2. Gunstad J, et al. (2007) Elevated body mass index is associated with executive dysfunction in otherwise healthy adults. Compr Psychiatry 48(1):57-61.
3. Smith E, Hay P, Campbell L, Trollor JN (2011) A review of the association between obesity and cognitive function across the lifespan: Implications for novel approaches to prevention and treatment. Obes Rev 12(9):740-755.
4. Taras H, Potts-Datema W (2005) Obesity and student performance at school. J Sch Health 75(8):291-295.
5. Yau PL, Castro MG, Tagani A, Tsui WH, Convit A (2012) Obesity and metabolic syndrome and functional and structural brain impairments in adolescence. Pediatrics 130(4):e856-e864.
6. Kidd PM (2008) Alzheimer's disease, amnestic mild cognitive impairment, and ageassociated memory impairment: Current understanding and progress toward integrative prevention. Altern Med Rev 13(2):85-115.
7. Ward MA, Carlsson CM, Trivedi MA, Sager MA, Johnson SC (2005) The effect of body mass index on global brain volume in middle-aged adults: A cross sectional study. BMC Neurol 5:23.
8. Pannacciulli N, et al. (2006) Brain abnormalities in human obesity: A voxel-based morphometric study. Neuroimage 31(4):1419-1425.
9. Raji CA, et al. (2010) Brain structure and obesity. Hum Brain Mapp 31(3):353-364.
10. Wessels AM, et al. (2007) Cognitive performance in type 1 diabetes patients is associated with cerebral white matter volume. Diabetologia 50(8):1763-1769.
11. Debette S, et al. (2011) Midlife vascular risk factor exposure accelerates structural brain aging and cognitive decline. Neurology 77(5):461-468.
12. Crichton GE, et al. (2012) Metabolic syndrome, cognitive performance, and dementia. J Alzheimers Dis 30(Suppl 2):S77-S87.
13. Meo SA, et al. (2013) Impact of type 1 diabetes mellitus on academic performance. J Int Med Res 41(3):855-858.
14. Hill JO, Peters JC (1998) Environmental contributions to the obesity epidemic. Science 280(5368):1371-1374.
15. Bagnol D, Al-Shamma HA, Behan D, Whelan K, Grottick AJ (2012) Diet-induced models of obesity (DIO) in rodents. Curr Protoc Neurosci Chapter 9(38):1-13.
16. Hendrickx H, McEwen BS, Ouderaa Fv (2005) Metabolism, mood and cognition in aging: The importance of lifestyle and dietary intervention. Neurobiol Aging 26(Suppl 1):1-5.
17. Allan CA, McLachlan RI (2010) Androgens and obesity. Curr Opin Endocrinol Diabetes Obes 17(3):224-232.
18. Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31(29):10721-10731.
19. Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20(11):4320-4324.
20. Ng CW, Noblejas MI, Rodefer JS, Smith CB, Poremba A (2007) Double dissociation of attentional resources: Prefrontal versus cingulate cortices. J Neurosci 27(45):12123-12131.
21. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: Neural and neurochemical substrates. Neurosci Biobehav Rev 28(7):771-784.
22. Crawley JN (1999) Behavioral phenotyping of transgenic and knockout mice: Experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res 835(1):18-26.
23. Yang M, Crawley JN (2009) Simple behavioral assessment of mouse olfaction. Curr Protoc Neurosci Chapter 8(8):24.
24. Watanabe Y, Gould E, McEwen BS (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588(2):341-345.
25. Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 94(18):9956-9961.
26. Thiel G (1993) Synapsin I, synapsin II, and synaptophysin: Marker proteins of synaptic vesicles. Brain Pathol 3(1):87-95.
27. Chaudhry FA, et al. (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18(23):9733-9750.
28. Fung SJ, Webster MJ, Weickert CS (2011) Expression of VGluT1 and VGAT mRNAs in human dorsolateral prefrontal cortex during development and in schizophrenia. Brain Res 1388:22-31.
29. Balschun D, et al. (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20(3):684-693.
30. Izant JG, McIntosh JR (1980) Microtubule-associated proteins: A monoclonal antibody to MAP2 binds to differentiated neurons. Proc Natl Acad Sci USA 77(8):4741-4745.
31. Aguzzi A, Barres BA, Bennett ML (2013) Microglia: Scapegoat, saboteur, or something else? Science 339(6116):156-161.
32. Stephan AH, Barres BA, Stevens B (2012) The complement system: An unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci 35:369-389.
33. Schafer DP, et al. (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691-705.
34. Paolicelli RC, et al. (2011) Synaptic pruning by microglia is necessary for normal brain development. Science 333(6048):1456-1458.
35. Karatsoreos IN, Bhagat S, Bloss EB, Morrison JH, McEwen BS (2011) Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci USA 108(4):1657-1662.
36. Apergis-Schoute J, Pinto A, Paré D (2006) Ultrastructural organization of medial prefrontal inputs to the rhinal cortices. Eur J Neurosci 24(1):135-144.
37. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tracttracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290(2):213-242.
38. Cerqueira JJ, Taipa R, Uylings HB, Almeida OF, Sousa N (2007) Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 17(9):1998-2006.
39. Mizoguchi K, Ishige A, Takeda S, Aburada M, Tabira T (2004) Endogenous glucocorticoids are essential for maintaining prefrontal cortical cognitive function. J Neurosci 24(24):5492-5499.
40. Doherty GH, Beccano-Kelly D, Yan SD, Gunn-Moore FJ, Harvey J (2013) Leptin prevents hippocampal synaptic disruption and neuronal cell death induced by amyloid β. Neurobiol Aging 34(1):226-237.
41. Oomura Y, et al. (2006) Leptin facilitates learning and memory performance and enhances hippocampal CA1 long-term potentiation and CaMK II phosphorylation in rats. Peptides 27(11):2738-2749.
42. O'Malley D, et al. (2007) Leptin promotes rapid dynamic changes in hippocampal dendritic morphology. Mol Cell Neurosci 35(4):559-572.
43. Hao S, Dey A, Yu X, Stranahan AM (2015) Dietary obesity reversibly induces synaptic stripping by microglia and impairs hippocampal plasticity. Brain Behav Immun, 10.1016/j.bbi.2015.08.023.
44. Kesby JP, et al. (2015) Spatial cognition in adult and aged mice exposed to high-fat diet. PLoS One 10(10):e0140034.
45. Baran SE, et al. (2005) Combination of high fat diet and chronic stress retracts hippocampal dendrites. Neuroreport 16(1):39-43.
46. Wellman CL (2001) Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 49(3):245-253.
47. Liston C, et al. (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26(30):7870-7874.
48. Liston C, et al. (2013) Circadian glucocorticoid oscillations promote learningdependent synapse formation and maintenance. Nat Neurosci 16(6):698-705.
49. Liston C, Gan WB (2011) Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci USA 108(38):16074-16079.
50. Volkow ND, et al. (2009) Inverse association between BMI and prefrontal metabolic activity in healthy adults. Obesity (Silver Spring) 17(1):60-65.
51. Brooks SJ, Cedernaes J, Schiöth HB (2013) Increased prefrontal and parahippocampal activation with reduced dorsolateral prefrontal and insular cortex activation to food images in obesity: A meta-analysis of fMRI studies. PLoS One 8(4):e60393.
52. Balodis IM, et al. (2013) Divergent neural substrates of inhibitory control in binge eating disorder relative to other manifestations of obesity. Obesity (Silver Spring) 21(2):367-377.
53. Shenhav A, Botvinick MM, Cohen JD (2013) The expected value of control: An integrative theory of anterior cingulate cortex function. Neuron 79(2):217-240.
54. National Research Council (2011) Guide for the Care and Use of Laboratory Animals (National Academies Press, Washington, DC), 8th Ed.