METABOLIC CONTROL OF HIGH-FREQUENCY GAMMA OSCILLATIONS IN THE BRAIN
https://doi.org/10.33647/2074-5982-15-2-43-53
Abstract
A high-frequency electrical activity across the range of 30–100 Hz, known as gamma rhythms, is observed in many regions of the brain. This phenomenon serves to synchronize the activity of various neural networks intended to process, transmit, store and receive information. Gamma rhythms play a key role in such processes of higher nervous activity as attention, sensory perception and memory formation. Impairment of gamma rhythms is a common symptom of diseases associated with cognitive impairment, including Alzheimer’s disease, epilepsy and schizophrenia. Recent studies have shown that a particular population of GABAergic-inhibiting neurons, i.e. parvalbumin-positive (PV+) interneurons, is the source of high-frequency oscillations. Maintenance of gamma rhythms is an extremely energy-intensive process that relies on a high rate of oxidative phosphorylation in the mitochondria of neurons and is limited by the presence of glucose. Insulin may be involved in the metabolic control of gamma oscillations, since PV+ interneurons selectively express the insulin-dependent glucose transporter GLUT4, which can provide an additional glucose influx under near-limit functioning conditions as in the case of high-frequency gamma oscillations. This review generalized available literature data on the relationship between metabolism and a high-frequency electrical brain activity, with an emphasis on the possible contribution of central insulin resistance to disturbances of gamma rhythms in the brain.
About the Authors
I. A. Pomytkin
I.M. Sechenov First Moscow State Medical University;
Scientific Center of Biomedical Technologies of the Federal Medical and Biological Agency of Russia
Russian Federation
Russian Federation
Cand. Sci. (Chem.),
119991, Russian Federation, Moscow, Trubetskaya str., 8/2
143442, Russian Federation, Moscow region, Krasnogorsk district, Settlement Svetlye Gory, building 1
N. N. Karkischenko
Scientific Center of Biomedical Technologies of the Federal Medical and Biological Agency of Russia
Russian Federation
Russian Federation
Dr. Sci. (Med.), Prof., Corresponding Member of the Russian Academy of Sciences, Academician of the Russian Academy of Rocket and Artillery Sciences
143442, Russian Federation, Moscow region, Krasnogorsk district, Settlement Svetlye Gory, building 1
References
1. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995;15(1 Pt 1):47–60.
2. Tort A.B., Kramer M.A., Thorn C., Gibson D.J., Kubota Y., Graybiel A.M., et al. Dynamic crossfrequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc. Natl Acad. Sci. USA. 2008;105(51):20517–22. DOI: 10.1073/pnas.0810524105.
3. Gray C.M., Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl Acad. Sci. USA. 1989;86(5):1698–1702.
4. Chrobak J.J., Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 1998;18(1):388–398.
5. Popescu A.T., Popa D., Paré D. Coherent gamma oscillations couple the amygdala and striatum during learning. Nat. Neurosci. 2009;12(6):801–807. DOI: 10.1038/nn.2305.
6. Popa D., Spolidoro M., Proville R.D., Guyon N., Belliveau L., Léna C. Functional role of the cerebellum in gamma-band synchronization of the sensory and motor cortices. J. Neurosci. 2013;33(15):6552–56. DOI: 10.1523/JNEUROSCI.5521-12.2013.
7. Pinault D., Deschênes M. Voltage-dependent 40-Hz oscillations in rat reticular thalamic neurons in vivo. Neuroscience. 1992;51(2):245–258.
8. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science. 2001;4:1259–64.
9. Zhang Z.G., Hu L., Hung Y.S., Mouraux A., Iannetti G.D. Gamma-band oscillations in the primary somatosensory cortex — a direct and obligatory correlate of subjective pain intensity. J. Neurosci. 2012;32(22):7429–38. DOI: 10.1523/JNEUROSCI.5877-11.2012.
10. Lisman J.E., Idiart M.A. Storage of 7 +/- 2 shortterm memories in oscillatory subcycles. Science. 1995;267(5203):1512–15.
11. de Almeida L., Idiart M., Lisman J.E. Memory retrieval time and memory capacity of the CA3 network: role of gamma frequency oscillations. Learn Mem. 2007;14(11):795–806.
12. Jensen O., Kaiser J., Lachaux J.P. Human gammafrequency oscillations associated with attention and memory. Trends Neurosci. 2007;30(7):317–324.
13. Buzsáki G., Wang X.J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012;35:203–225.
14. Wilson H.R., Cowan J.D. Excitatory and inhibitory interactions in localized populations of model neurons. Biophys. J. 1972;12(1):1–24.
15. Leung L.S. Nonlinear feedback model of neuronal populations in hippocampal CAl region. J. Neurophysiol. 1982;47(5):845–868.
16. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. 1995;373(6515):612–615.
17. Salkoff D.B., Zagha E., Yüzgeç Ö., McCormick D.A. Synaptic Mechanisms of Tight Spike Synchrony at Gamma Frequency in Cerebral Cortex. J. Neurosci. 2015;35(28):10236–51.
18. Pantev C., Makeig S., Hoke M., Galambos R., Hampson S., Gallen C. Human auditory evoked gamma-band magnetic fields. Proc. Natl Acad. Sci. USA. 1991;88(20):8996–9000.
19. Lehmann D., Faber P.L., Achermann P., Jeanmonod D., Gianotti L.R., Pizzagalli D. Brain sources of EEG gamma frequency during volitionally meditation-induced, altered states of consciousness, and experience of the self. Psychiatry Res. 2001;108(2):111–121.
20. Lutz A., Greischar L.L., Rawlings N.B., Ricard M., Davidson R.J. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proc. Natl Acad. Sci. USA. 2004;101(46):16369–73.
21. Kann O., Papageorgiou I.E., Draguhn A. Highly energized inhibitory interneurons are a central element for information processing in cortical networks. J. Cereb. Blood Flow Metab. 2014;34(8):1270–82. DOI: 10.1038/jcbfm.2014.104.
22. Galow L.V., Schneider J., Lewen A., Ta T.T., Papageorgiou I.E., Kann O. Energy substrates that fuel fast neuronal network oscillations. Front Neurosci. 2014;8:398. DOI: 10.3389/fnins.2014.00398.
23. Tremblay R., Lee S., Rudy B. GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits. Neuron. 2016;91(2):260–292. DOI: 10.1016/j.neuron.2016.06.033.
24. Celio M.R., Heizmann C.W. Calcium-binding protein parvalbumin as a neuronal marker. Nature. 1981;293(5830):300–302.
25. Celio M.R. Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science. 1986;231(4741):995–997.
26. Collin T., Chat M., Lucas M.G., Moreno H., Racay P., Schwaller B., et al. Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J. Neurosci. 2005;25(1):96–107.
27. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex. 1997;7(6):476–486.
28. Kann O. The interneuron energy hypothesis: Implications for brain disease. Neurobiol. Dis. 2016;90:75–85. DOI: 10.1016/j.nbd.2015.08.005.
29. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007;8(1):45–56.
30. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 2009;459(7247):698–702. DOI: 10.1038/nature07991.
31. Gulyás A.I., Szabó G.G., Ulbert I., Holderith N., Monyer H., Erdélyi F., et al. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J. Neurosci. 2010;30(45):15134–45. DOI: 10.1523/JNEUROSCI.4104-10.2010.
32. Packer A.M., Yuste R. Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J. Neurosci. 2011;31(37):13260–71. DOI: 10.1523/ JNEUROSCI.3131-11.2011.
33. Hu H., Gan J., Jonas P. Interneurons. Fast-spiking, parvalbumin+GABAergic interneurons: from cellular design to microcircuit function. Science. 2014;345(6196):1255263. DOI: 10.1126/science.1255263.
34. Schwaller B. Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol. 2010;2(11):a004051. DOI: 10.1101/cshperspect.a004051.
35. Kann O., Huchzermeyer C., Kovács R., Wirtz S., Schuelke M. Gamma oscillations in the hippocampus require high complex I gene expression and strong functional performance of mitochondria. Brain. 2011;134(Pt 2):345–358. DOI: 10.1093/brain/awq333.
36. Huchzermeyer C., Albus K., Gabriel H.J., Otáhal J., Taubenberger N., Heinemann U., et al. Gamma oscillations and spontaneous network activity in the hippocampus are highly sensitive to decreases in pO2 and concomitant changes in mitochondrial redox state. J. Neurosci. 2008;28(5):1153–62. DOI: 10.1523/JNEUROSCI.4105-07.2008.
37. Kann O., Hollnagel J.O., Elzoheiry S., Schneider J. Energy and Potassium Ion Homeostasis during Gamma Oscillations. Front. Mol. Neurosci. 2016;9:47. DOI: 10.3389/fnmol.2016.00047.
38. Huchzermeyer C., Berndt N., Holzhütter H.G., Kann O. Oxygen consumption rates during three different neuronal activity states in the hippocampal CA3 network. J. Cereb. Blood Flow Metab. 2013;33(2):263–271. DOI: 10.1038/jcbfm.2012.165.
39. Lukyanova L.D., Kirova Y.I. Mitochondria-controlled signaling mechanisms of brain protection in hypoxia. Front. Neurosci. 2015;9:320. DOI: 10.3389/fnins.2015.00320.
40. Schneider J., Lewen A., Ta T.T., Galow L.V., Isola R., Papageorgiou I.E., et al. A reliable model for gamma oscillations in hippocampal tissue. J. Neurosci. Res. 2015;93(7):1067–78. DOI: 10.1002/jnr.23590.
41. Cataldo A.M., Broadwell R.D. Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions. II. Choroid plexus and ependymal epithelia, endothelia and pericytes. J. Neurocytol. 1986;15(4):511–524.
42. Calì C., Tauffenberger A., Magistretti P. The Strategic Location of Glycogen and Lactate: From Body Energy Reserve to Brain Plasticity. Front. Cell Neurosci. 2019;13:82. DOI: 10.3389/fncel.2019.00082.
43. Saez I., Duran J., Sinadinos C., Beltran A., Yanes O., Tevy M.F., et al. Neurons have an active glycogen metabolism that contributes to tolerance to hypoxia. J. Cereb. Blood Flow Metab. 2014;34(6):945–955. DOI: 10.1038/jcbfm.2014.33.
44. Suzuki A., Stern S.A., Bozdagi O., Huntley G.W., Walker R.H., Magistretti P.J., et al. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell. 2011;144(5):810–823. DOI: 10.1016/j.cell.2011.02.018.
45. Lai J.C., Walsh J.M., Dennis S.C., Clark J.B. Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J. Neurochem. 1977;28(3):625–631.
46. Simpson I.A., Dwyer D., Malide D., Moley K.H., Travis A., Vannucci S.J. The facilitative glucose transporter GLUT3: 20 years of distinction. Am. J. Physiol. Endocrinol. Metab. 2008;295(2):E242–E253. DOI: 10.1152/ajpendo.90388.2008.
47. Colville C.A., Seatter M.J., Jess T.J., Gould G.W., Thomas H.M. Kinetic analysis of the liver-type (GLUT2) and brain-type (GLUT3) glucose transporters in Xenopus oocytes: substrate specificities and effects of transport inhibitors. Biochem. J. 1993;290(Pt 3):701–706.
48. Bröer S., Bröer A., Schneider H.P., Stegen C., Halestrap A.P., Deitmer J.W. Characterization of the high-affinity monocarboxylate transporter MCT2 in Xenopus laevis oocytes. Biochem. J. 1999;341(Pt 3):529–535.
49. Nishimura H., Pallardo F.V., Seidner G.A., Vannucci S., Simpson I.A., Birnbaum M.J. Kinetics of GLUT1 and GLUT4 glucose transporters expressed in Xenopus oocytes. J. Biol. Chem. 1993;268(12):8514–20.
50. El Messari S., Leloup C., Quignon M., Brisorgueil M.J., Penicaud L., Arluison M. Immunocytochemical localization of the insulin-responsive glucose transporter 4 (Glut4) in the rat central nervous system. J. Comp. Neurol. 1998;399(4):492–512.
51. Apelt J., Mehlhorn G., Schliebs R. Insulin-sensitive GLUT4 glucose transporters are colocalized with GLUT3-expressing cells and demonstrate a chemically distinct neuron-specific localization in rat brain. J. Neurosci. Res. 1999;57(5):693–705.
52. Grillo C.A., Piroli G.G., Hendry R.M., Reagan L.P. Insulin-stimulated translocation of GLUT4 to the plasma membrane in rat hippocampus is PI3-kinase dependent. Brain Res. 2009;1296:35–45. DOI: 10.1016/j.brainres.2009.08.005.
53. Pearson-Leary J., Jahagirdar V., Sage J., McNay E.C. Insulin modulates hippocampally-mediated spatial working memory via glucose transporter-4. Behav. Brain Res. 2018;338:32–39. DOI: 10.1016/j. bbr.2017.09.033.
54. Tikhonova T.B., Miyamae T., Gulchina Y., Lewis D.A., Gonzalez-Burgos G. Cell Type- and Layer-Specific Muscarinic Potentiation of Excitatory Synaptic Drive onto Parvalbumin Neurons in Mouse Prefrontal Cortex. eNeuro. 2018;5(5). pii: ENEURO.0208-18.2018. DOI: 10.1523/ ENEURO.0208-18.2018.
55. Palovcik R.A., Phillips M.I., Kappy M.S., Raizada M.K. Insulin inhibits pyramidal neurons in hippocampal slices. Brain Res. 1984;309(1):187–191.
56. Kurudenkandy F.R., Zilberter M., Biverstål H., Presto J., Honcharenko D., Strömberg R., et al. Amyloid-β-induced action potential desynchronization and degradation of hippocampal gamma oscillations is prevented by interference with peptide conformation change and aggregation. J. Neurosci. 2014;34(34):11416–25. DOI: 10.1523/JNEUROSCI.1195-14.2014.
57. Simpson I.A., Chundu K.R., Davies-Hill T., Honer W.G., Davies P. Decreased concentrations of GLUT1 and GLUT3 glucose transporters in the brains of patients with Alzheimer’s disease. Ann. Neurol. 1994;35(5):546–551.
58. Pearson-Leary J., McNay E.C. Intrahippocampal administration of amyloid-β(1-42) oligomers acutely impairs spatial working memory, insulin signaling, and hippocampal metabolism. J. Alzheimers Dis. 2012;30(2):413–422. DOI: 10.3233/JAD-2012-112192.
59. Oliveira L.T., Leon G.V.O., Provance D.W. Jr, de Mello F.G., Sorenson M.M., Salerno V.P. Exogenous β-amyloid peptide interferes with GLUT4 localization in neurons. Brain Res. 2015;1615:42–50. DOI: 10.1016/j.brainres.2015.04.026.
60. Talbot K., Wang H.Y., Kazi H., Han L.Y., Bakshi K.P., Stucky A., et al. Demonstrated brain insulin resistance in Alzheimer’s disease patients is associated with IGF1 resistance, IRS-1 dysregulation, and cognitive decline. J. Clin. Invest. 2012;122(4):1316–38. DOI: 10.1172/JCI59903.
61. Verret L., Mann E.O., Hang G.B., Barth A.M., Cobos I., Ho K., et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell. 2012;149(3):708–721. DOI: 10.1016/j.cell.2012.02.046.
62. Başar E., Femir B., Emek-Savaş D.D., Güntekin B., Yener G.G. Increased long distance event-related gamma band connectivity in Alzheimer’s disease. Neuroimage Clin. 2017;14:580–590. DOI: 10.1016/j.nicl.2017.02.021.
63. Başar E., Ozesmi C. The hippocampal EEG-activity and a systems analytical interpretation of averaged evoked potentials of the brain. Kybernetik. 1972;12(1):45–54.
64. Başar E. A review of gamma oscillations in healthy subjects and in cognitive impairment. Int. J. Psychophysiol. 2013;90(2):99–117. DOI: 10.1016/j.ijpsycho.2013.07.005.
65. Başar E., Emek-Savaş D.D., Güntekin B., Yener G.G. Delay of cognitive gamma responses in Alzheimer’s disease. Neuroimage Clin. 2016;11:106–115. DOI: 10.1016/j.nicl.2016.01.015.
Review
For citations:
Pomytkin I.A., Karkischenko N.N. METABOLIC CONTROL OF HIGH-FREQUENCY GAMMA OSCILLATIONS IN THE BRAIN. Journal Biomed. 2019;(2):43-53. (In Russ.) https://doi.org/10.33647/2074-5982-15-2-43-53
Views:
788
Email this article 
