Table of Contents
International Journal of Peptides
Volume 2017 (2017), Article ID 7386809, 9 pages
https://doi.org/10.1155/2017/7386809
Research Article

Amyloid β Peptide-Induced Changes in Prefrontal Cortex Activity and Its Response to Hippocampal Input

Departamento de Neurobiología del Desarrollo y Neurofisiología, Instituto de Neurobiología, Universidad Nacional Autónoma de México, 76230 Querétaro, QRO, Mexico

Correspondence should be addressed to Fernando Peña-Ortega; xm.manu@anepfj

Received 18 June 2016; Accepted 2 November 2016; Published 3 January 2017

Academic Editor: Per Hellström

Copyright © 2017 Ernesto Flores-Martínez and Fernando Peña-Ortega. 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. J. W. Dalley, R. N. Cardinal, and T. W. Robbins, “Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates,” Neuroscience and Biobehavioral Reviews, vol. 28, no. 7, pp. 771–784, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. P. S. Goldman-Rakic, “Cellular basis of working memory,” Neuron, vol. 14, no. 3, pp. 477–485, 1995. View at Publisher · View at Google Scholar · View at Scopus
  3. R. P. Kesner and J. C. Churchwell, “An analysis of rat prefrontal cortex in mediating executive function,” Neurobiology of Learning and Memory, vol. 96, no. 3, pp. 417–431, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. B. P. Godsil, J. P. Kiss, M. Spedding, and T. M. Jay, “The hippocampal-prefrontal pathway: the weak link in psychiatric disorders?” European Neuropsychopharmacology, vol. 23, no. 10, pp. 1165–1181, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. A. D. Baddeley, S. Bressi, S. Della Sala, R. Logie, and H. Spinnler, “The decline of working memory in Alzheimer's disease: A Longitudinal Study,” Brain, vol. 114, no. 6, pp. 2521–2542, 1991. View at Publisher · View at Google Scholar · View at Scopus
  6. E. A. Kensinger, D. K. Shearer, J. J. Locascio, J. H. Growdon, and S. Corkin, “Working memory in mild Alzheimer's disease and early Parkinson's disease,” Neuropsychology, vol. 17, no. 2, pp. 230–239, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. C. R. Jack Jr., V. J. Lowe, M. L. Senjem et al., “11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment,” Brain, vol. 131, no. 3, pp. 665–680, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Mori, H. Shimada, H. Shinotoh et al., “Apathy correlates with prefrontal amyloid β deposition in Alzheimer's disease,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 85, no. 4, pp. 449–455, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. J.-M. Zhuo, A. Prakasam, M. E. Murray et al., “An increase in Aβ42 in the prefrontal cortex is associated with a reversal-learning impairment in Alzheimer's disease model Tg2576 APPsw mice,” Current Alzheimer Research, vol. 5, no. 4, pp. 385–391, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Blanchard, G. Martel, L. Brayda-Bruno, X. Noguès, and J. Micheau, “Detection of age-dependent working memory deterioration in APP751SL mice,” Behavioural Brain Research, vol. 218, no. 1, pp. 129–137, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. C. Lo, E. Iscru, D. Blum et al., “Amyloid and tau neuropathology differentially affect prefrontal synaptic plasticity and cognitive performance in mouse models of Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 37, no. 1, pp. 109–125, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Bories, M. J. Guitton, C. Julien et al., “Sex-dependent alterations in social behaviour and cortical synaptic activity coincide at different ages in a model of Alzheimer's disease,” PLoS ONE, vol. 7, no. 9, article e46111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. É. Proulx, P. Fraser, J. McLaurin, and E. K. Lambe, “Impaired cholinergic excitation of prefrontal attention circuitry in the TgCRND8 model of Alzheimer’s disease,” Journal of Neuroscience, vol. 35, no. 37, pp. 12779–12791, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Platt, B. Drever, D. Koss et al., “Abnormal cognition, sleep, eeg and brain metabolism in a novel knock-in alzheimer mouse, plb1,” PLoS ONE, vol. 6, no. 11, article e27068, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Zhong, Z. Gu, X. Wang, H. Jiang, J. Feng, and Z. Yan, “Impaired modulation of GABAergic transmission by muscarinic receptors in a mouse transgenic model of Alzheimer's disease,” The Journal of Biological Chemistry, vol. 278, no. 29, pp. 26888–26896, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. W. Liu, F. Dou, J. Feng, and Z. Yan, “RACK1 is involved in β-amyloid impairment of muscarinic regulation of GABAergic transmission,” Neurobiology of Aging, vol. 32, no. 10, pp. 1818–1826, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. G.-J. Chen, Z. Xiong, and Z. Yan, “Aβ impairs nicotinic regulation of inhibitory synaptic transmission and interneuron excitability in prefrontal cortex,” Molecular Neurodegeneration, vol. 8, no. 1, article 3, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. W. Bai, H. Yi, T. Liu, J. Wei, and X. Tian, “Incoordination between spikes and LFPs in Aβ1-42-mediated memory deficits in rats,” Frontiers in Behavioral Neuroscience, vol. 8, article 411, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Wei, H. Yi, D. Zhang, W. Bai, and X. Tian, “Aberrant neuronal activity and dysfunctional connectivity in Aβ1-42 mediated memory deficits in rats,” Current Alzheimer Research, vol. 12, no. 10, pp. 964–973, 2015. View at Publisher · View at Google Scholar
  20. P. Faucher, N. Mons, J. Micheau, C. Louis, and D. J. Beracochea, “Hippocampal injections of oligomeric amyloid β-peptide (1–42) induce selective working memory deficits and long-lasting alterations of ERK signaling pathway,” Frontiers in Aging Neuroscience, vol. 7, article 245, 2016. View at Publisher · View at Google Scholar
  21. D. B. Carr and S. R. Sesack, “Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopamine terminals,” Journal of Comparative Neurology, vol. 369, no. 1, pp. 1–15, 1996. View at Publisher · View at Google Scholar · View at Scopus
  22. T. M. Jay, A.-M. Thierry, L. Wiklung, and J. Glowinski, “Excitatory amino acid pathway from the hippocampus to the prefrontal cortex. Contribution of AMPA receptors in hippocampo-prefrontal cortex transmission,” European Journal of Neuroscience, vol. 4, no. 12, pp. 1285–1295, 1992. View at Publisher · View at Google Scholar · View at Scopus
  23. M. A. Parent, L. Wang, J. Su, T. Netoff, and L.-L. Yuan, “Identification of the hippocampal input to medial prefrontal cortex in vitro,” Cerebral Cortex, vol. 20, no. 2, pp. 393–403, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Gabbott, A. Headlam, and S. Busby, “Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat,” Brain Research, vol. 946, no. 2, pp. 314–322, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. P. L. Tierney, E. Dégenètais, A.-M. Thierry, J. Glowinski, and Y. Gioanni, “Influence of the hippocampus on interneurons of the rat prefrontal cortex,” European Journal of Neuroscience, vol. 20, no. 2, pp. 514–524, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. M. W. Jones and M. A. Wilson, “Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task,” PLoS Biology, vol. 3, no. 12, article e402, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. J. M. Hyman, E. A. Zilli, A. M. Paley, and M. E. Hasselmo, “Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates,” Frontiers in Integrative Neuroscience, vol. 4, p. 2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Sigurdsson, K. L. Stark, M. Karayiorgou, J. A. Gogos, and J. A. Gordon, “Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia,” Nature, vol. 464, no. 7289, pp. 763–767, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Wang, Y. Zang, Y. He et al., “Changes in hippocampal connectivity in the early stages of Alzheimer's disease: evidence from resting state fMRI,” NeuroImage, vol. 31, no. 2, pp. 496–504, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. S. Goveas, C. Xie, B. D. Ward et al., “Recovery of hippocampal network connectivity correlates with cognitive improvement in mild Alzheimer's disease patients treated with donepezil assessed by resting-state fMRI,” Journal of Magnetic Resonance Imaging, vol. 34, no. 4, pp. 764–773, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Zarei, C. F. Beckmann, M. A. Binnewijzend et al., “Functional segmentation of the hippocampus in the healthy human brain and in Alzheimer's disease,” Neuroimage, vol. 66, pp. 28–35, 2013. View at Publisher · View at Google Scholar
  32. N. Maingret, G. Girardeau, R. Todorova, M. Goutierre, and M. Zugaro, “Hippocampo-cortical coupling mediates memory consolidation during sleep,” Nature Neuroscience, vol. 19, no. 7, pp. 959–964, 2016. View at Publisher · View at Google Scholar
  33. A. G. Isla, F. G. Vázquez-Cuevas, F. Peña-Ortega, and S. Krantic, “Exercise prevents amyloid-β-induced hippocampal network disruption by inhibiting GSK3β activation,” Journal of Alzheimer's Disease, vol. 52, no. 1, pp. 333–343, 2016. View at Publisher · View at Google Scholar
  34. H. Balleza-Tapia, A. Huanosta-Gutiérrez, A. Márquez-Ramos, N. Arias, and F. Peña, “Amyloid β oligomers decrease hippocampal spontaneous network activity in an age-dependent manner,” Current Alzheimer Research, vol. 7, no. 5, pp. 453–462, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Adaya-Villanueva, B. Ordaz, H. Balleza-Tapia, A. Márquez-Ramos, and F. Peña-Ortega, “Beta-like hippocampal network activity is differentially affected by amyloid beta peptides,” Peptides, vol. 31, no. 9, pp. 1761–1766, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Peña, J. Bargas, and R. Tapia, “Paired pulse facilitation is turned into paired pulse depression in hippocampal slices after epilepsy induced by 4-aminopyridine in vivo,” Neuropharmacology, vol. 42, no. 6, pp. 807–812, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Peña, B. Ordaz, H. Balleza-Tapia et al., “Beta-amyloid protein (25–35) disrupts hippocampal network activity: role of Fyn-kinase,” Hippocampus, vol. 20, no. 1, pp. 78–96, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. V. Vargas-Barroso, B. Ordaz-Sánchez, F. Peña-Ortega, and J. A. Larriva-Sahd, “Electrophysiological evidence for a direct link between the main and accessory olfactory bulbs in the adult rat,” Frontiers in Neuroscience, vol. 9, article 518, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Ramírez, J. Hernández-Montoya, S. L. Sánchez-Serrano et al., “GABA-mediated induction of early neuronal markers expression in postnatal rat progenitor cells in culture,” Neuroscience, vol. 224, pp. 210–222, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. L. Carrillo-Reid, F. Tecuapetla, D. Tapia et al., “Encoding network states by striatal cell assemblies,” Journal of Neurophysiology, vol. 99, no. 3, pp. 1435–1450, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Pérez-Ortega, M. Duhne, E. Lara-González et al., “Pathophysiological signatures of functional connectomics in parkinsonian and dyskinetic striatal microcircuits,” Neurobiology of Disease, vol. 91, pp. 347–361, 2016. View at Publisher · View at Google Scholar
  42. M. E. Stone, A. Maffei, and A. Fontanini, “Amygdala stimulation evokes time-varying synaptic responses in the gustatory cortex of anesthetized rats,” Frontiers in Integrative Neuroscience, vol. 5, article 3, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Alvarado-Martínez, K. Salgado-Puga, and F. Peña-Ortega, “Amyloid beta inhibits olfactory bulb activity and the ability to smell,” PLoS ONE, vol. 8, no. 9, Article ID e75745, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. F. Peña-Ortega, Á. Solis-Cisneros, B. Ordaz, H. Balleza-Tapia, and J. J. López-Guerrero, “Amyloid beta 1–42 inhibits entorhinal cortex activity in the beta-gamma range: role of GSK-3,” Current Alzheimer Research, vol. 9, no. 7, pp. 857–863, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. F. R. Kurudenkandy, M. Zilberter, H. Biverstål et al., “Amyloid-β-induced action potential desynchronization and degradation of hippocampal gamma oscillations is prevented by interference with peptide conformation change and aggregation,” The Journal of Neuroscience, vol. 34, no. 34, pp. 11416–11425, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Wang, G. Zhang, H. Zhou, A. Barakat, and H. Querfurth, “Opposite effects of low and high doses of Aβ42 on electrical network and neuronal excitability in the rat prefrontal cortex,” PLoS ONE, vol. 4, no. 12, article e8366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. V. Nimmrich, C. Grimm, A. Draguhn et al., “Amyloid β oligomers (Aβ1–42 globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents,” Journal of Neuroscience, vol. 28, no. 4, pp. 788–797, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. C. Xing, Y. Yin, R. Chang, X. He, and Z. Xie, “A role of insulin-like growth factor 1 in β amyloid-induced disinhibition of hippocampal neurons,” Neuroscience Letters, vol. 384, no. 1-2, pp. 93–97, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Montez, S.-S. Poil, B. F. Jones et al., “Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 5, pp. 1614–1619, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. F. Peña-Ortega and R. Bernal-Pedraza, “Amyloid beta peptide slows down sensory-induced hippocampal oscillations,” International Journal of Peptides, vol. 2012, Article ID 236289, 8 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. A. I. Gutiérrez-Lerma, B. Ordaz, and F. Peña-Ortega, “Amyloid beta peptides differentially affect hippocampal theta rhythms in vitro,” International Journal of Peptides, vol. 2013, Article ID 328140, 11 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. S. H. Bitzenhofer, K. Sieben, K. D. Siebert, M. Spehr, and I. L. Hanganu-Opatz, “Oscillatory activity in developing prefrontal networks results from theta-gamma-modulated synaptic inputs,” Cell Reports, vol. 11, no. 3, pp. 486–497, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. K. M. Igarashi, “Plasticity in oscillatory coupling between hippocampus and cortex,” Current Opinion in Neurobiology, vol. 35, pp. 163–168, 2015. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Verret, E. O. Mann, G. B. Hang et al., “Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in alzheimer model,” Cell, vol. 149, no. 3, pp. 708–721, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Peña-Ortega, “Amyloid beta-protein and neural network dysfunction,” Journal of Neurodegenerative Diseases, vol. 2013, Article ID 657470, 8 pages, 2013. View at Publisher · View at Google Scholar
  56. E. C. W. Van Straaten, P. Scheltens, A. A. Gouw, and C. J. Stam, “Eyes-closed task-free electroencephalography in clinical trials for Alzheimer's disease: an emerging method based upon brain dynamics,” Alzheimer's Research and Therapy, vol. 6, no. 9, article 86, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. M. M. Engels, A. Hillebrand, W. M. van der Flier, C. J. Stam, P. Scheltens, and E. C. van Straaten, “Slowing of hippocampal activity correlates with cognitive decline in early onset Alzheimer's disease. An MEG study with virtual electrodes,” Frontiers in Human Neuroscience, vol. 10, article 238, 2016. View at Publisher · View at Google Scholar
  58. J. E. Driver, C. Racca, M. O. Cunningham et al., “Impairment of hippocampal gamma (γ)-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP),” European Journal of Neuroscience, vol. 26, no. 5, pp. 1280–1288, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Goutagny, N. Gu, C. Cavanagh et al., “Alterations in hippocampal network oscillations and theta-gamma coupling arise before Aβ overproduction in a mouse model of Alzheimer's disease,” European Journal of Neuroscience, vol. 37, no. 12, pp. 1896–1902, 2013. View at Google Scholar
  60. H. Balleza-Tapia and F. Peña, “Pharmacology of the intracellular pathways activated by amyloid beta protein,” Mini-Reviews in Medicinal Chemistry, vol. 9, no. 6, pp. 724–740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Salgado-Puga, R. A. Prado-Alcalá, and F. Peña-Ortega, “Amyloid β enhances typical rodent behavior while it impairs contextual memory consolidation,” Behavioural Neurology, vol. 2015, Article ID 526912, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Salgado-Puga and F. Peña-Ortega, “Cellular and network mechanisms underlying memory impairment induced by amyloid β protein,” Protein and Peptide Letters, vol. 22, no. 4, pp. 303–321, 2015. View at Publisher · View at Google Scholar · View at Scopus