A reliable model for gamma oscillations in hippocampal tissue

Journal of Neuroscience Research

Volumn 93, Issue 7, 2015, Pages 1067-1078

  Schneider, Justus ^a   Lewen, Andrea ^a   Ta, Thuy Truc ^a   Galow, Lukas V ^a   Isola, Raffaella ^a,b   Papageorgiou, Ismini E ^a,c   Kann, Oliver ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF CAGLIARI   (Italy)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Electrophysiology; Energy metabolism; Hippocampus; Inhibitory interneuron; Lactate

Indexed keywords

ACETYLCHOLINE; GLUCOSE; AMINO ACID RECEPTOR AFFECTING AGENT; CHOLINERGIC RECEPTOR STIMULATING AGENT; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN TISSUE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGICAL PROCEDURES; ELECTROPHYSIOLOGY; ENERGY METABOLISM; GAMMA OSCILLATION; GAMMA RHYTHM; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; IN VITRO STUDY; INTERNEURON; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SLICE CULTURE; AGE; ANIMAL; DRUG EFFECTS; METABOLISM; NEWBORN; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; TEMPERATURE; TIME; WISTAR RAT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CHOLINERGIC AGENTS; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGENTS; GAMMA RHYTHM; GLUCOSE; HIPPOCAMPUS; IN VITRO TECHNIQUES; ORGAN CULTURE TECHNIQUES; PARVALBUMINS; RATS; RATS, WISTAR; TEMPERATURE; TIME FACTORS;

EID: 84929631164     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23590     Document Type: Article

References (66)

1. Bahr BA, Kessler M, Rivera S, Vanderklish PW, Hall RA, Mutneja MS, Gall C, Hoffman KB. 1995. Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus 5:425-439.
2. Bak LK, Schousboe A, Waagepetersen HS. 2006. The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis, and ammonia transfer. J Neurochem 98:641-653.
3. Barros LF. 2013. Metabolic signaling by lactate in the brain. Trends Neurosci 36:396-404.
4. Bartos M, Vida I, Jonas P. 2007. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45-56.
5. Bergersen LH. 2015. Lactate transport and signaling in the brain: potential therapeutic targets and roles in body-brain interaction. J Cereb Blood Flow Metab 35:176-185.
6. 2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22:10593-10602.
7. Bischofberger J, Engel D, Li L, Geiger JRP, Jonas P. 2006. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1:2075-2081.
8. Bouzier-Sore A-K, Voisin P, Canioni P, Magistretti PJ, Pellerin L. 2003. Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 23:1298-1306.
9. Caeser M, Aertsen A. 1991. Morphological organization of rat hippocampal slice cultures. J Comp Neurol 307:87-106.
10. De Simoni A, Griesinger CB, Edwards FA. 2003. Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 550:135-147.
11. 2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels. J Neurosci 31:13676-13681.
12. Dickinson R, Awaiz S, Whittington MA, Lieb WR, Franks NP. 2003. The effects of general anaesthetics on carbachol-evoked gamma oscillations in the rat hippocampus in vitro. Neuropharmacology 44:864-872.
13. Dienel GA. 2012. Brain lactate metabolism: the discoveries and the controversies. J Cereb Blood Flow Metab 32:1107-1138.
14. Egorov AV, Draguhn A. 2013. Development of coherent neuronal activity patterns in mammalian cortical networks: common principles and local hetereogeneity. Mech Dev 130:412-423.
15. Fellous J-M, Sejnowski TJ. 2000. Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus 10:187-197.
16. Fisahn A, Pike FG, Buhl EH, Paulsen O. 1998. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
17. Fisahn A, Yamada M, Duttaroy A, Gan J-W, Deng C-X, McBain CJ, Wess J. 2002. Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33:615-624.
18. Fischer V, Both M, Draguhn A, Egorov AV. 2014. Choline-mediated modulation of hippocampal sharp wave-ripple complexes in vitro. J Neurochem 129:792-805.
19. Fischer Y, Wittner L, Freund TF, Gähwiler BH. 2002. Simultaneous activation of gamma and theta network oscillations in rat hippocampal slice cultures. J Physiol 539:857-868.
20. Galow LV, Schneider J, Lewen A, Ta T-T, Papageorgiou IE, Kann O. 2014. Energy substrates that fuel fast neuronal network oscillations. Front Neurosci 8:398.
21. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH. 2005. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. J Physiol 562:131-147.
22. Gulyás AI, Buzsáki G, Freund TF, Hirase H. 2006. Populations of hippocampal inhibitory neurons express different levels of cytochrome c. Eur J Neurosci 23:2581-2594.
23. Gulyás AI, Szabó GG, Ulbert I, Holderith N, Monyer H, Erdélyi F, Szabó G, Freund TF, Hájos N. 2010. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30:15134-15145.
24. Hájos N, Mody I. 2009. Establishing a physiological environment for visualized in vitro brain slice recordings by increasing oxygen supply and modifying aCSF content. J Neurosci Methods 183:107-113.
25. Hájos N, Paulsen O. 2009. Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Netw 22:1113-1119.
26. Hájos N, Papp EC, Acsády L, Levey AI, Freund TF. 1998. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82:355-376.
27. Hájos N, Pálhalmi J, Mann EO, Németh B, Paulsen O, Freund TF. 2004. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24:9127-9137.
28. Hájos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O. 2009. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29:319-327.
29. + channels ensures fast signaling in GABAergic interneuron axons. Nat Neurosci 17:686-693.
30. 2 and concomitant changes in mitochondrial redox state. J Neurosci 28:1153-1162.
31. Huchzermeyer C, Berndt N, Holzhütter H-G, Kann O. 2013. Oxygen consumption rates during three different neuronal activity states in the hippocampal CA3 network. J Cereb Blood Flow Metab 33:263-271.
32. Ivanov A, Mukhtarov M, Bregestovski P, Zilberter Y. 2011. Lactate effectively covers energy demands during neuronal network activity in neonatal hippocampal slices. Front Neuroenergetics 3:2.
33. Kann O. 2012. The energy demand of fast neuronal network oscillations: insights from brain slice preparations. Front Pharmacol 2:90.
34. Kann O, Kovács R. 2007. Mitochondria and neuronal activity. Am J Physiol Cell Physiol 292:C641-C657.
35. 2+ and stimulates oxidative metabolism in hippocampal slice cultures. J Neurophysiol 90:613-621.
36. Kann O, Schuchmann S, Buchheim K, Heinemann U. 2003b. Coupling of neuronal activity and mitochondrial metabolism as revealed by NAD(P)H fluorescence signals in organotypic hippocampal slice cultures of the rat. Neuroscience 119:87-100.
37. Kann O, Huchzermeyer C, Kovács R, Wirtz S, Schuelke M. 2011. Gamma oscillations in the hippocampus require high complex I gene expression and strong functional performance of mitochondria. Brain 134:345-358.
38. Kann O, Papageorgiou IE, Draguhn A. 2014. Highly energized inhibitory interneurons are a central element for information processing in cortical networks. J Cereb Blood Flow Metab 34:1270-1282.
39. Kasischke KA, Lambert EM, Panepento B, Sun A, Gelbard HA, Burgess RW, Foster TH, Nedergaard M. 2011. Two-photon NADH imaging exposes boundaries of oxygen diffusion in cortical vascular supply regions. J Cereb Blood Flow Metab 31:68-81.
40. Lauritzen KH, Morland C, Puchades M, Holm-Hansen S, Hagelin EM, Lauritzen F, Attramadal H, Storm-Mathisen J, Gjedde A, Bergersen LH. 2014. Lactate receptor sites link neurotransmission, neurovascular coupling, and brain energy metabolism. Cereb Cortex 24:2784-2795.
41. Lehmann D, Faber PL, Achermann P, Jeanmonod D, Gianotti LRR, Pizzagalli D. 2001. Brain sources of EEG gamma frequency during volitionally meditation-induced, altered states of consciousness, and experience of the self. Psychiatry Res 108:111-121.
42. Li C-L, McIlwain H. 1957. Maintenance of resting membrane potentials in slices of mammalian cerebral cortex and other tissues in vitro. J Physiol 139:178-190.
43. Lutz A, Greischar LL, Rawlings NB, Ricard M, Davidson RJ. 2004. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proc Natl Acad Sci U S A 101:16369-16373.
44. Marrosu F, Portas C, Mascia MS, Casu MA, Fà M, Giagheddu M, Imperato A, Gessa GL. 1995. Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671:329-332.
45. Montgomery SM, Buzsáki G. 2007. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci U S A 104:14495-14500.
46. Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RAW. 2005. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948-951.
47. Nishida M, Juhász C, Sood S, Chugani HT, Asano E. 2008. Cortical glucose metabolism positively correlates with gamma-oscillations in nonlesional focal epilepsy. Neuroimage 42:1275-1284.
48. Oren I, Hájos N, Paulsen O. 2010. Identification of the current generator underlying cholinergically induced gamma frequency field potential oscillations in the hippocampal CA3 region. J Physiol 588:785-797.
49. Paulsen O, Moser EI. 1998. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci 21:273-278.
50. Penttonen M, Kamondi A, Acsády L, Buzsáki G. 1998. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10:718-728.
51. Pietersen ANJ, Patel N, Jefferys JGR, Vreugdenhil M. 2009. Comparison between spontaneous and kainate-induced gamma oscillations in the mouse hippocampus in vitro. Eur J Neurosci 29:2145-2156.
52. Pomper JK, Graulich J, Kovacs R, Hoffmann U, Gabriel S, Heinemann U. 2001. High oxygen tension leads to acute cell death in organotypic hippocampal slice cultures. Brain Res Dev Brain Res 126:109-116.
53. Schurr A, Payne RS. 2007. Lactate, not pyruvate, is neuronal aerobic glycolysis end product: an in vitro electrophysiological study. Neuroscience 147:613-619.
54. Schurr A, West CA, Rigor BM. 1988. Lactate-supported synaptic function in the rat hippocampal slice preparation. Science 240:1326-1328.
55. Simpson IA, Carruthers A, Vannucci SJ. 2007. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J Cereb Blood Flow Metab 27:1766-1791.
56. Sonnewald U. 2014. Glutamate synthesis has to be matched by its degradation-where do all the carbons go? J Neurochem 131:399-406.
57. Stoppini L, Buchs P-A, Muller D. 1991. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
58. Studer D, Zhao S, Chai X, Jonas P, Graber W, Nestel S, Frotscher M. 2014. Capture of activity-induced ultrastructural changes at synapses by high-pressure freezing of brain tissue. Nat Protoc 9:1480-1495.
59. Suzuki A, Stern SA, Bozdagi O, Huntley GW, Walker RH, Magistretti PJ, Alberini CM. 2011. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell 144:810-823.
60. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JGR. 1996. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493:471-484.
61. Uhlhaas PJ, Singer W. 2010. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:100-113.
62. van Vugt MK, Schulze-Bonhage A, Litt B, Brandt A, Kahana MJ. 2010. Hippocampal gamma oscillations increase with memory load. J Neurosci 30:2694-2699.
63. Vovenko E. 1999. Distribution of oxygen tension on the surface of arterioles, capillaries, and venules of brain cortex and in tissue in normoxia: an experimental study on rats. Pflügers Arch 437:617-623.
64. Whittington MA, Traub RD. 2003. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 26:676-682.
65. Wójtowicz AM, van den Boom L, Chakrabarty A, Maggio N, ul Haq R, Behrens CJ, Heinemann U. 2009. Monoamines block kainate- and carbachol-induced γ-oscillations but augment stimulus-induced γ-oscillations in rat hippocampus in vitro. Hippocampus 19:273-288.
66. Zhao S, Studer D, Chai X, Graber W, Brose N, Nestel S, Young C, Rodriguez EP, Saetzler K, Frotscher M. 2012. Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. J Comp Neurol 520:2340-2351.