Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2015, Article ID 657928, 10 pages
http://dx.doi.org/10.1155/2015/657928
Review Article

Modulation of Hippocampal Neural Plasticity by Glucose-Related Signaling

Institute of Human Physiology, Medical School, Università Cattolica, Largo Francesco Vito 1, 00168 Rome, Italy

Received 30 December 2014; Revised 2 April 2015; Accepted 5 April 2015

Academic Editor: Michel Baudry

Copyright © 2015 Marco Mainardi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. J. M. Verberne, A. Sabetghadam, and W. S. Korim, “Neural pathways that control the glucose counterregulatory response,” Frontiers in Neuroscience, no. 8, article 38, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. K. W. Williams and J. K. Elmquist, “From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior,” Nature Neuroscience, vol. 15, no. 10, pp. 1350–1355, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. S. D. Jordan, A. C. Könner, and J. C. Brüning, “Sensing the fuels: glucose and lipid signaling in the CNS controlling energy homeostasis,” Cellular and Molecular Life Sciences, vol. 67, no. 19, pp. 3255–3273, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Folli, S. Ghidella, L. Bonfanti, C. R. Kahn, and A. Merighi, “The early intracellular signaling pathway for the insulin/insulin-like growth factor receptor family in the mammalian central nervous system,” Molecular Neurobiology, vol. 13, no. 2, pp. 155–183, 1996. View at Publisher · View at Google Scholar · View at Scopus
  5. J.-I. Hwang, S. Yun, M. J. Moon, C. R. Park, and J. Y. Seong, “MOlecular evolution of GPCRs: GLP1/GLP1 receptors,” Journal of Molecular Endocrinology, vol. 52, no. 3, pp. T15–T27, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Fusco and G. Pani, “Brain response to calorie restriction,” Cellular and Molecular Life Sciences, vol. 70, no. 17, pp. 3157–3170, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Howarth, P. Gleeson, and D. Attwell, “Updated energy budgets for neural computation in the neocortex and cerebellum,” Journal of Cerebral Blood Flow and Metabolism, vol. 32, no. 7, pp. 1222–1232, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. M. V. Ivannikov, M. Sugimori, and R. R. Llinás, “Calcium clearance and its energy requirements in cerebellar neurons,” Cell Calcium, vol. 47, no. 6, pp. 507–513, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. G. A. Dienel, “Fueling and imaging brain activation,” ASN Neuro, vol. 4, no. 5, pp. 267–321, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. D. Y. Kim, I. Rhee, and J. Paik, “Metabolic circuits in neural stem cells,” Cellular and Molecular Life Sciences, vol. 71, no. 21, pp. 4221–4241, 2014. View at Publisher · View at Google Scholar
  11. L. Hertz and M. E. Gibbs, “What learning in day-old chickens can teach a neurochemist: focus on astrocyte metabolism,” Journal of Neurochemistry, vol. 109, supplement 1, pp. 10–16, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Suzuki, S. A. Stern, O. Bozdagi et al., “Astrocyte-neuron lactate transport is required for long-term memory formation,” Cell, vol. 144, no. 5, pp. 810–823, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. I. A. Simpson, A. Carruthers, and S. J. Vannucci, “Supply and demand in cerebral energy metabolism: the role of nutrient transporters,” Journal of Cerebral Blood Flow and Metabolism, vol. 27, no. 11, pp. 1766–1791, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. E. Blazquez, E. Velazquez, V. Hurtado-Carneiro et al., “Insulin in the brain: its pathophysiological implications for States related with central insulin resistance, type 2 diabetes and Alzheimer's disease,” Frontiers in Endocrinology (Lausanne), vol. 5, article 161, 2014. View at Google Scholar
  15. A. M. Fernandez and I. Torres-Alemán, “The many faces of insulin-like peptide signalling in the brain,” Nature Reviews Neuroscience, vol. 13, no. 4, pp. 225–239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. J. J. Holst, “The physiology of glucagon-like peptide 1,” Physiological Reviews, vol. 87, no. 4, pp. 1409–1439, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Hölscher and A. Hamilton, “Receptors for the incretin glucagon-like peptide-1 are expressed on neurons in the central nervous system,” NeuroReport, vol. 20, no. 13, pp. 1161–1166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Merchenthaler, M. Lane, and P. Shughrue, “Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system,” Journal of Comparative Neurology, vol. 403, no. 2, pp. 261–280, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. M. J. During, L. Cao, D. S. Zuzga et al., “Glucagon-like peptide-1 receptor is involved in learning and neuroprotection,” Nature Medicine, vol. 9, no. 9, pp. 1173–1179, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. Z. B. Andrews and A. Abizaid, “Neuroendocrine mechanisms that connect feeding behavior and stress,” Frontiers in Neuroscience, vol. 8, article 312, 2014. View at Publisher · View at Google Scholar
  21. F. Broglio, E. Arvat, A. Benso et al., “Ghrelin, a natural gh secretagogue produced by the stomach, induces hyperglycemia and reduces insulin secretion in humans,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 10, pp. 5083–5086, 2001. View at Publisher · View at Google Scholar · View at Scopus
  22. J. N. Cuellar and M. Isokawa, “Ghrelin-induced activation of cAMP signal transduction and its negative regulation by endocannabinoids in the hippocampus,” Neuropharmacology, vol. 60, no. 6, pp. 842–851, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. L. M. Frago, E. Baquedano,, J. Argente, and J. A. Chowen, “Neuroprotective actions of ghrelin and growth hormone secretagogues,” Frontiers in Molecular Neuroscience, vol. 4, article 28, 2011. View at Publisher · View at Google Scholar
  24. L. F. Ribeiro, T. Catarino, S. D. Santos et al., “Ghrelin triggers the synaptic incorporation of AMPA receptors in the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 1, pp. E149–E158, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. L. F. Reichardt, “Neurotrophin-regulated signalling pathways,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 361, no. 1473, pp. 1545–1564, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Y. Altarejos and M. Montminy, “CREB and the CRTC co-activators: sensors for hormonal and metabolic signals,” Nature Reviews Molecular Cell Biology, vol. 12, no. 3, pp. 141–151, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Finkbeiner, “CREB couples neurotrophin signals to survival messages,” Neuron, vol. 25, no. 1, pp. 11–14, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Fusco, G. Maulucci, and G. Pani, “Sirt1: def-eating senescence?” Cell Cycle, vol. 11, no. 22, pp. 4135–4146, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. L.-L. Du, J.-Z. Xie, X.-S. Cheng et al., “Activation of sirtuin 1 attenuates cerebral ventricular streptozotocin-induced tau hyperphosphorylation and cognitive injuries in rat hippocampi,” Age, vol. 36, no. 2, pp. 613–623, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Jeong, D. E. Cohen, L. Cui et al., “Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway,” Nature Medicine, vol. 18, no. 1, pp. 159–165, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Fusco, C. Ripoli, M. V. Podda et al., “A role for neuronal cAMP responsive-element binding (CREB)-1 in brain responses to calorie restriction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 2, pp. 621–626, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. D. E. Cohen, A. M. Supinski, M. S. Bonkowski et al., “Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction,” Genes & Development, vol. 23, no. 24, pp. 2812–2817, 2009. View at Google Scholar
  33. J. Gao, W.-Y. Wang, Y.-W. Mao et al., “A novel pathway regulates memory and plasticity via SIRT1 and miR-134,” Nature, vol. 466, no. 7310, pp. 1105–1109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Liu, Z. Zhao, F. Yang, Y. Gao, J. Song, and Y. Wan, “microRNA-181a is involved in insulin-like growth factor-1-mediated regulation of the transcription factor CREB1,” Journal of Neurochemistry, vol. 126, no. 6, pp. 771–780, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Choeiri, W. Staines, T. Miki, S. Seino, and C. Messier, “Glucose transporter plasticity during memory processing,” Neuroscience, vol. 130, no. 3, pp. 591–600, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Kamal, G. M. J. Ramakers, W. H. Gispen, G. J. Biessels, and A. Al Ansari, “Hyperinsulinemia in rats causes impairment of spatial memory and learning with defects in hippocampal synaptic plasticity by involvement of postsynaptic mechanisms,” Experimental Brain Research, vol. 226, no. 1, pp. 45–51, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Nisticó, V. Cavallucci, S. Piccinin et al., “Insulin receptor β-subunit haploinsufficiency impairs hippocampal late-phase ltp and recognition memory,” NeuroMolecular Medicine, vol. 14, no. 4, pp. 262–269, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Kerti, A. V. Witte, A. Winkler, U. Grittner, D. Rujescu, and A. Flöel, “Higher glucose levels associated with lower memory and reduced hippocampal microstructure,” Neurology, vol. 81, no. 20, pp. 1746–1752, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Chen, O. Charlat, L. A. Tartaglia et al., “Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice,” Cell, vol. 84, no. 3, pp. 491–495, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. A. M. Stranahan, K. Lee, B. Martin et al., “Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice,” Hippocampus, vol. 19, no. 10, pp. 951–961, 2009. View at Google Scholar
  41. R. Agrawal, Y. Zhuang, B. P. Cummings et al., “Deterioration of plasticity and metabolic homeostasis in the brain of the UCD-T2DM rat model of naturally occurring type-2 diabetes,” Biochimica et Biophysica Acta—Molecular Basis of Disease, vol. 1842, no. 9, pp. 1313–1323, 2014. View at Publisher · View at Google Scholar
  42. M.-H. Kim, J. Choi, J. Yang et al., “Enhanced NMDA receptor-mediated synaptic transmission, enhanced long-term potentiation, and impaired learning and memory in mice lacking IRSp53,” Journal of Neuroscience, vol. 29, no. 5, pp. 1586–1595, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. E. E. Irvine, L. Drinkwater, K. Radwanska et al., “Insulin receptor substrate 2 is a negative regulator of memory formation,” Learning & Memory, vol. 18, no. 6, pp. 375–383, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Boitard, N. Etchamendy, J. Sauvant et al., “Juvenile, but not adult exposure to high-fat diet impairs relational memory and hippocampal neurogenesis in mice,” Hippocampus, vol. 22, no. 11, pp. 2095–2100, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Mainardi, G. Scabia, T. Vottari et al., “A sensitive period for environmental regulation of eating behavior and leptin sensitivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 38, pp. 16673–16678, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Berardi, T. Pizzorusso, and L. Maffei, “Critical periods during sensory development,” Current Opinion in Neurobiology, vol. 10, no. 1, pp. 138–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. J. I. Trejo, J. Piriz, M. V. Llorens-Martin et al., “Central actions of liver-derived insulin-like growth factor I underlying its pro-cognitive effects,” Molecular Psychiatry, vol. 12, no. 12, pp. 1118–1128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Svensson, M. Diez, J. Engel et al., “Endocrine, liver-derived IGF-I is of importance for spatial learning and memory in old mice,” Journal of Endocrinology, vol. 189, no. 3, pp. 617–627, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. B. Lupien, E. J. Bluhm, and D. N. Ishii, “Systemic insulin-like growth factor-I administration prevents cognitive impairment in diabetic rats, and brain IGF regulates learning/memory in normal adult rats,” Journal of Neuroscience Research, vol. 74, no. 4, pp. 512–523, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Diano, S. A. Farr, S. C. Benoit et al., “Ghrelin controls hippocampal spine synapse density and memory performance,” Nature Neuroscience, vol. 9, no. 3, pp. 381–388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. L. Chen, T. Xing, M. Wang et al., “Local infusion of ghrelin enhanced hippocampal synaptic plasticity and spatial memory through activation of phosphoinositide 3-kinase in the dentate gyrus of adult rats,” European Journal of Neuroscience, vol. 33, no. 2, pp. 266–275, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Abbas, E. Faivre, and C. Hölscher, “Impairment of synaptic plasticity and memory formation in GLP-1 receptor KO mice: interaction between type 2 diabetes and Alzheimer's disease,” Behavioural Brain Research, vol. 205, no. 1, pp. 265–271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Isacson, E. Nielsen, K. Dannaeus et al., “The glucagon-like peptide 1 receptor agonist exendin-4 improves reference memory performance and decreases immobility in the forced swim test,” European Journal of Pharmacology, vol. 650, no. 1, pp. 249–255, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. S. M. G. Braun and S. Jessberger, “Review: adult neurogenesis and its role in neuropsychiatric disease, brain repair and normal brain function,” Neuropathology and Applied Neurobiology, vol. 40, no. 1, pp. 3–12, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. N. Urbán and F. Guillemot, “Neurogenesis in the embryonic and adult brain: same regulators, different roles,” Frontiers in Cellular Neuroscience, vol. 8, article 396, 2014. View at Publisher · View at Google Scholar
  56. E. Castilla-Ortega, C. Pedraza, G. Estivill-Torrús, and L. J. Santín, “When is adult hippocampal neurogenesis necessary for learning? Evidence from animal research,” Reviews in the Neurosciences, vol. 22, no. 3, pp. 267–283, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. S. W. Lee, G. D. Clemenson, and F. H. Gage, “New neurons in an aged brain,” Behavioural Brain Research, vol. 227, no. 2, pp. 497–507, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. C. J. Taylor, D. J. Jhaveri, and P. F. Bartlett, “The therapeutic potential of endogenous hippocampal stem cells for the treatment of neurological disorders,” Frontiers in Cellular Neuroscience, vol. 7, article 5, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. M. A. I. Åberg, N. D. Åberg, T. D. Palmer et al., “IGF-I has a direct proliferative effect in adult hippocampal progenitor cells,” Molecular and Cellular Neuroscience, vol. 24, no. 1, pp. 23–40, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. G. J. F. Brooker, M. Kalloniatis, V. C. Russo, M. Murphy, G. A. Werther, and P. F. Bartlett, “Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells,” Journal of Neuroscience Research, vol. 59, no. 3, pp. 332–341, 2000. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Drago, M. Murphy, S. M. Carroll, R. P. Harvey, and P. F. Bartlett, “Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 6, pp. 2199–2203, 1991. View at Publisher · View at Google Scholar · View at Scopus
  62. J. M. Chell and A. H. Brand, “Nutrition-responsive glia control exit of neural stem cells from quiescence,” Cell, vol. 143, no. 7, pp. 1161–1173, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Sousa-Nunes, L. L. Yee, and A. P. Gould, “Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila,” Nature, vol. 471, no. 7339, pp. 508–513, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Y. Sun, “Hippocampal IGF-1 expression, neurogenesis and slowed aging: clues to longevity from mutant mice,” Age, vol. 28, no. 2, pp. 181–189, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Lee, K. B. Seroogy, and M. P. Mattson, “Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice,” Journal of Neurochemistry, vol. 80, no. 3, pp. 539–547, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. P. K. Dash, S. A. Mach, and A. N. Moore, “Enhanced neurogenesis in the rodent hippocampus following traumatic brain injury,” Journal of Neuroscience Research, vol. 63, no. 4, pp. 313–319, 2001. View at Google Scholar · View at Scopus
  67. N. Maswood, J. Young, E. Tilmont et al., “Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 52, pp. 18171–18176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Saharan, D. J. Jhaveri, and P. F. Bartlett, “SIRT1 regulates the neurogenic potential of neural precursors in the adult subventricular zone and hippocampus,” Journal of Neuroscience Research, vol. 91, no. 5, pp. 642–659, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Ma, M. Yao, Q. Zhai, J. Jiao, X. Yuan, and M. Poo, “SIRT1 suppresses self-renewal of adult hippocampal neural stem cells,” Development, vol. 141, no. 24, pp. 4697–4709, 2014. View at Publisher · View at Google Scholar
  70. T. Prozorovski, U. Schulze-Topphoff, R. Glumm et al., “Sirt1 contributes critically to the redox-dependent fate of neural progenitors,” Nature Cell Biology, vol. 10, no. 4, pp. 385–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. V. M. Renault, V. A. Rafalski, A. A. Morgan et al., “FoxO3 regulates neural stem cell homeostasis,” Cell Stem Cell, vol. 5, no. 5, pp. 527–539, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. L. Magri, M. Cambiaghi, M. Cominelli et al., “Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions,” Cell Stem Cell, vol. 9, no. 5, pp. 447–462, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. V. A. Gault and C. Hölscher, “GLP-1 agonists facilitate hippocampal LTP and reverse the impairment of LTP induced by beta-amyloid,” European Journal of Pharmacology, vol. 587, no. 1–3, pp. 112–117, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. C.-C. Lee, C.-C. Huang, and K.-S. Hsu, “Insulin promotes dendritic spine and synapse formation by the PI3K/Akt/mTOR and Rac1 signaling pathways,” Neuropharmacology, vol. 61, no. 4, pp. 867–879, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. L. P. van der Heide, A. Kamal, A. Artola, W. H. Gispen, and G. M. J. Ramakers, “Insulin modulates hippocampal activity-dependent synaptic plasticity in a N-methyl-D-aspartate receptor and phosphatidyl-inositol-3-kinase-dependent manner,” Journal of Neurochemistry, vol. 94, no. 4, pp. 1158–1166, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. W. C. Abraham, “Metaplasticity: tuning synapses and networks for plasticity,” Nature Reviews Neuroscience, vol. 9, no. 5, pp. 387–399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. V. A. Skeberdis, J.-Y. Lan, X. Zheng, R. S. Zukin, and M. V. L. Bennett, “Insulin promotes rapid delivery of N-methyl-d-aspartate receptors to the cell surface by exocytosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 6, pp. 3561–3566, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. J. M. Christie, R. J. Wenthold, and D. T. Monaghan, “Insulin causes a transient tyrosine phosphorylation of NR2A and NR2B NMDA receptor subunits in rat hippocampus,” Journal of Neurochemistry, vol. 72, no. 4, pp. 1523–1528, 1999. View at Publisher · View at Google Scholar · View at Scopus
  79. L. Liu, J. C. Brown III, W. W. Webster, R. A. Morrisett, and D. T. Monaghan, “Insulin potentiates N-methyl-d-aspartate receptor activity in Xenopus oocytes and rat hippocampus,” Neuroscience Letters, vol. 192, no. 1, pp. 5–8, 1995. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Barria and R. Malinow, “NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII,” Neuron, vol. 48, no. 2, pp. 289–301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. A. C. Gambrill and A. Barria, “NMDA receptor subunit composition controls synaptogenesis and synapse stabilization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 14, pp. 5855–5860, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. L. Adzovic and L. Domenici, “Insulin induces phosphorylation of the AMPA receptor subunit GluR1, reversed by ZIP, and over-expression of Protein Kinase M zeta, reversed by amyloid beta,” Journal of Neurochemistry, vol. 131, no. 5, pp. 582–587, 2014. View at Publisher · View at Google Scholar
  83. D. Plitzko, S. Rumpel, and K. Gottmann, “Insulin promotes functional induction of silent synapses in differentiating rat neocortical neurons,” European Journal of Neuroscience, vol. 14, no. 8, pp. 1412–1415, 2001. View at Publisher · View at Google Scholar · View at Scopus
  84. A. Kamal, G. M. J. Ramakers, W. H. Gispen, and G. J. Biessels, “Effect of chronic intracerebroventricular insulin administration in rats on the peripheral glucose metabolism and synaptic plasticity of CA1 hippocampal neurons,” Brain Research, vol. 1435, pp. 99–104, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. M.-A. Abbott, D. G. Wells, and J. R. Fallon, “The insulin receptor tyrosine kinase substrate p58/53 and the insulin receptor are components of CNS synapses,” The Journal of Neuroscience, vol. 19, no. 17, pp. 7300–7308, 1999. View at Google Scholar · View at Scopus
  86. H. Miki, H. Yamaguchi, S. Suetsugu, and T. Takenawa, “IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling,” Nature, vol. 408, no. 6813, pp. 732–735, 2000. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Choi, J. Ko, B. Racz et al., “Regulation of dendritic spine morphogenesis by insulin receptor substrate 53, a downstream effector of Rac1 and Cdc42 small GTPases,” Journal of Neuroscience, vol. 25, no. 4, pp. 869–879, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Sawallisch, K. Berhörster, A. Disanza et al., “The insulin receptor substrate of 53 kDa (IRSp53) limits hippocampal synaptic plasticity,” The Journal of Biological Chemistry, vol. 284, no. 14, pp. 9225–9236, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. E. D. Martín, A. Sánchez-Perez, J. L. Trejo et al., “IRS-2 deficiency impairs NMDA receptor-dependent long-term potentiation,” Cerebral Cortex, vol. 22, no. 8, pp. 1717–1727, 2012. View at Publisher · View at Google Scholar · View at Scopus
  90. A. P. Corvin, I. Molinos, G. Little et al., “Insulin-like growth factor 1 (IGF1) and its active peptide (1–3)IGF1 enhance the expression of synaptic markers in neuronal circuits through different cellular mechanisms,” Neuroscience Letters, vol. 520, no. 1, pp. 51–56, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. C. M. Cheng, R. F. Mervis, S.-L. Niu et al., “Insulin-like growth factor 1 is essential for normal dendritic growth,” Journal of Neuroscience Research, vol. 73, no. 1, pp. 1–9, 2003. View at Publisher · View at Google Scholar · View at Scopus
  92. E. R. Glasper, M. V. Llorens-Martin, B. Leuner, E. Gould, and J. L. Trejo, “Blockade of insulin-like growth factor-I has complex effects on structural plasticity in the hippocampus,” Hippocampus, vol. 20, no. 6, pp. 706–712, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. J. R. O'Kusky, P. Ye, and A. J. D'Ercole, “Insulin-like growth factor-I promotes neurogenesis and synaptogenesis in the hippocampal dentate gyrus during postnatal development,” Journal of Neuroscience, vol. 20, no. 22, pp. 8435–8442, 2000. View at Google Scholar · View at Scopus
  94. K. Talbot, H.-Y. Wang, H. Kazi et al., “Demonstrated brain insulin resistance in Alzheimer's disease patients is associated with IGF-1 resistance, IRS-1 dysregulation, and cognitive decline,” The Journal of Clinical Investigation, vol. 122, no. 4, pp. 1316–1338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  95. L. Berrout and M. Isokawa, “Ghrelin promotes reorganization of dendritic spines in cultured rat hippocampal slices,” Neuroscience Letters, vol. 516, no. 2, pp. 280–284, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. Z. F. Mainen, M. Maletic-Savatic, S. H. Shi, Y. Hayashi, R. Malinow, and K. Svoboda, “Two-photon imaging in living brain slices,” Methods, vol. 18, no. 2, pp. 231–239, 1999. View at Publisher · View at Google Scholar · View at Scopus
  97. L. Shi, X. Bian, Z. Qu et al., “Peptide hormone ghrelin enhances neuronal excitability by inhibition of Kv7/KCNQ channels,” Nature Communications, vol. 4, article 1435, 2013. View at Publisher · View at Google Scholar · View at Scopus
  98. S. V. Korol, Z. Jin, O. Babateen, and B. Birnir, “GLP-1 and exendin-4 transiently enhance GABAA receptor-mediated synaptic and tonic currents in rat hippocampal CA3 pyramidal neurons,” Diabetes, vol. 64, no. 1, pp. 79–89, 2014. View at Publisher · View at Google Scholar
  99. C. P. Gilman, T. A. Perry, K. Furukawa, N. H. Grieg, J. M. Egan, and M. P. Mattson, “Glucagon-like peptide 1 modulates calcium responses to glutamate and membrane depolarization in hippocampal neurons,” Journal of Neurochemistry, vol. 87, no. 5, pp. 1137–1144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. J.-I. Oka, N. Goto, and T. Kameyama, “Glucagon-like peptide-1 modulates neuronal activity in the rat's hippocampus,” NeuroReport, vol. 10, no. 8, pp. 1643–1646, 1999. View at Publisher · View at Google Scholar · View at Scopus
  101. C. T. Kodl and E. R. Seaquist, “Cognitive dysfunction and diabetes mellitus,” Endocrine Reviews, vol. 29, no. 4, pp. 494–511, 2008. View at Publisher · View at Google Scholar · View at Scopus
  102. M. F. Elias, A. L. Goodell, and S. R. Waldstein, “Obesity, cognitive functioning and dementia: back to the future,” Journal of Alzheimer's Disease, vol. 30, no. 2, pp. S113–S125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. K. S. Sellbom and J. Gunstad, “Cognitive function and decline in obesity,” Journal of Alzheimer's Disease, vol. 30, supplement 2, pp. S89–S95, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. B. Martin, S. Ji, S. Maudsley, and M. P. Mattson, “‘Control’ laboratory rodents are metabolically morbid: why it matters,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 14, pp. 6127–6133, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. N. J. Kirk-Sanchez and E. L. McGough, “Physical exercise and cognitive performance in the elderly: current perspectives,” Clinical Interventions in Aging, vol. 9, pp. 51–62, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. T. Cukierman-Yaffee, “The relationship between dysglycemia and cognitive dysfunction,” Current Opinion in Investigational Drugs, vol. 10, no. 1, pp. 70–74, 2009. View at Google Scholar · View at Scopus
  107. P. K. Crane, R. Walker, and E. B. Larson, “Glucose levels and risk of dementia,” The New England Journal of Medicine, vol. 369, no. 19, pp. 1863–1864, 2013. View at Publisher · View at Google Scholar
  108. M. Brownlee, “Biochemistry and molecular cell biology of diabetic complications,” Nature, vol. 414, no. 6865, pp. 813–820, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. W. Farris, S. Mansourian, Y. Chang et al., “Insulin-degrading enzyme regulates the levels of insulin, amyloid β-protein, and the β-amyloid precursor protein intracellular domain in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4162–4167, 2003. View at Publisher · View at Google Scholar · View at Scopus
  110. E. Steen, B. M. Terry, E. J. Rivera et al., “Impaired insulin and insulin-like growth factor expression and signaling mechanisms in Alzheimer's disease—is this type 3 diabetes?” Journal of Alzheimer's Disease, vol. 7, no. 1, pp. 63–80, 2005. View at Google Scholar · View at Scopus
  111. A. M. Stranahan, T. V. Arumugam, R. G. Cutler, K. Lee, J. M. Egan, and M. P. Mattson, “Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons,” Nature Neuroscience, vol. 11, no. 3, pp. 309–317, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. J. J. Ramos-Rodriguez, S. Molina-Gil, O. Ortiz-Barajas et al., “Central proliferation and neurogenesis is impaired in type 2 diabetes and prediabetes animal models,” PLoS ONE, vol. 9, no. 2, Article ID e89229, 2014. View at Publisher · View at Google Scholar
  113. M. A. Daulatzai, “Chronic functional bowel syndrome enhances gut-brain axis dysfunction, neuroinflammation, cognitive impairment, and vulnerability to dementia,” Neurochemical Research, vol. 39, no. 4, pp. 624–644, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. G. Clarke, S. Grenham, P. Scully et al., “The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner,” Molecular Psychiatry, vol. 18, no. 6, pp. 666–673, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Sale, N. Berardi, and L. Maffei, “Environment and brain plasticity: towards an endogenous pharmacotherapy,” Physiological Reviews, vol. 94, no. 1, pp. 189–234, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Mainardi, A. di Garbo, M. Caleo, N. Berardi, A. Sale, and L. Maffei, “Environmental enrichment strengthens corticocortical interactions and reduces amyloid-β oligomers in aged mice,” Frontiers in Aging Neuroscience, vol. 6, article 1, 2014. View at Publisher · View at Google Scholar
  117. H. van Praag, M. Fleshner, M. W. Schwartz, and M. P. Mattson, “Exercise, energy intake, glucose homeostasis, and the brain,” Journal of Neuroscience, vol. 34, no. 46, pp. 15139–15149, 2014. View at Publisher · View at Google Scholar
  118. W.-Q. Zhao, H. Chen, M. J. Quon, and D. L. Alkon, “Insulin and the insulin receptor in experimental models of learning and memory,” European Journal of Pharmacology, vol. 490, no. 1–3, pp. 71–81, 2004. View at Publisher · View at Google Scholar · View at Scopus
  119. A. J. Irving and J. Harvey, “Leptin regulation of hippocampal synaptic function in health and disease,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1633, Article ID 20130155, 2014. View at Google Scholar
  120. M. Mainardi, T. Pizzorusso, and M. Maffei, “Environment, leptin sensitivity, and hypothalamic plasticity,” Neural Plasticity, vol. 2013, Article ID 438072, 8 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus