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Region-dependent regulation of acute ethanol on γ oscillation in the rat hippocampal slices

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Abstract

Background

Ethanol use disorders are a serious medical and public health problem in the world today. Acute ethanol intoxication can lead to cognitive dysfunction such as learning and memory impairment. Gamma oscillations (γ, 30–80 Hz) are synchronized rhythmic activity generated by population of neurons within local network, and closely related to learning and memory function. The hippocampus is a critical anatomic structure that supports learning and memory. On the grounds of structure and function, hippocampus can be divided into the intermediate (IH), the dorsal (DH), and ventral hippocampus (VH). The current study is the first to investigate the effects of acute ethanol on γ oscillations in these sub-regions of rat hippocampal slices.

Methods

The sustained γ oscillations were induced by 200 nM kainate (KA) in the CA3c of IH, DH, and VH. When KA-induced γ oscillation reached the steady state, ethanol (50 mM or 100 mM) was applied and the effects of ethanol on γ oscillation power was measured in the slices sequentially sectioned from ventral to dorsal hippocampus of adult rats.

Results

In the intermediate hippocampal slices, compared with control (KA only), ethanol (50 mM) caused 36.1 ± 3.9% decrease in γ power (p < 0.05, n = 10), while ethanol (100 mM) caused 55.3 ± 5.5% decrease in γ power (p < 0.001, n = 14). In the dorsal hippocampus, only ethanol (100 mM) caused 18.1 ± 8.6% decrease in γ power (p < 0.05, n = 12). However, in the ventral hippocampus, neither 50 mM nor 100 mM ethanol affected γ oscillation.

Conclusions

Our results demonstrate that ethanol may produce the differential suppression of γ oscillations in a dose-dependent manner in different sub-regions of hippocampus, suggesting that the modulation of ethanol on hippocampal γ oscillation is region-dependent.

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References

  • Ariwodola OJ, Weiner JL (2004) Ethanol potentiation of GABAergic synaptic transmission may be self-limiting: role of presynaptic GABA(B) receptors. J Neurosci 24(47):10679–10686

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bast T (2007) Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior. Rev Neurosci 18:253–282

    PubMed  Google Scholar 

  • Bast T, Wilson IA, Witter MP, Morris RGM (2009) From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol 7(4):e1000089

    PubMed  PubMed Central  Google Scholar 

  • Blitzer RD, Gil O, Landau EM (1990) Long-term potentiation in rat hippocampus is inhibited by low concentrations of ethanol. Brain Res 537(1–2):203–208

    CAS  PubMed  Google Scholar 

  • Bocarsly ME, da Silva e Silva D, Kolb V, Luderman KD, Shashikiran S, Rubinstein M, Sibley DR, Dobbs LK, Alvarez VA (2019) A mechanism linking two known vulnerability factors for alcohol abuse: heightened alcohol stimulation and low striatal dopamine D2 receptors. Cell Rep 29(5):1147–1163.e5

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burwell RD (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911:25–42

    CAS  PubMed  Google Scholar 

  • Campbell AE, Sumner P, Singh KD, Muthukumaraswamy SD (2014) Acute effects of alcohol on stimulus-induced gamma oscillations in human primary visual and motor cortices. Neuropsychopharmacology 39(9):2104–2113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cenquizca LA, Swanson LW (2007) Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 56(1):1–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colgin LL (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17(4):239–249

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coller JK, Hutchinson MR (2012) Implications of central immune signaling caused by drugs of abuse: mechanisms, mediators and new therapeutic approaches for prediction and treatment of drug dependence. Pharmacol Ther 134(2):219–245

    CAS  PubMed  Google Scholar 

  • Dubovyk V, Manahan-Vaughan D (2019) Gradient of expression of dopamine D2 receptors along the dorso-ventral axis of the hippocampus. Front Synaptic Neurosci 11:28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65(1):7–19

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrani-Kile K, Randall PK, Leslie SW (2003) Acute ethanol affects phosphorylation state of the NMDA receptor complex: implication of tyrosine phosphatases and protein kinase a. Brain Res Mol Brain Res 115(1):78–86

    CAS  PubMed  Google Scholar 

  • Flentke GR, Garic A, Hernandez M, Smith SM (2014) CaMKII represses transcriptionally active beta-catenin to mediate acute ethanol neurodegeneration and can phosphorylate beta-catenin. J Neurochem 128(4):523–535

    CAS  PubMed  Google Scholar 

  • Fries P, Nikolic D, Singer W (2007) The gamma cycle. Trends Neurosci 30(7):309–316

    CAS  PubMed  Google Scholar 

  • Fuster-Matanzo A et al (2011) Different susceptibility to neurodegeneration of dorsal and ventral hippocampal dentate gyrus: a atudy with transgenic mice overexpressing GSK3β. PLoS One 6(11):e27262

  • Harper C (1998) The neuropathology of alcohol-specific brain damage, or does alcohol damage the brain? J Neuropathol Exp Neurol 57(2):101–110

    CAS  PubMed  Google Scholar 

  • Hoffmann SE, Matthews DB (2001) Ethanol-induced impairments in spatial working memory are not due to deficits in learning. Alcohol Clin Exp Res 25(6):856–861

    CAS  PubMed  Google Scholar 

  • Ishizuka N (2001) Laminar organization of the pyramidal cell layer of the subiculum in the rat. J Comp Neurol 435(1):89–110

    CAS  PubMed  Google Scholar 

  • Izumi Y, Nagashima K, Murayama K, Zorumski CF (2005) Acute effects of ethanol on hippocampal long-term potentiation and long-term depression are mediated by different mechanisms. Neuroscience 136(2):509–517

    CAS  PubMed  Google Scholar 

  • Jiang H et al (2020) Distinct directional couplings between slow and fast gamma power to the phase of theta oscillations in the rat hippocampus. Eur J Neurosci 51(10):2070–2081

  • Kemp A, Manahan-Vaughan D (2007) Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci 30(3):111–118

    CAS  PubMed  Google Scholar 

  • Kenney J, Manahan-Vaughan D (2013) Learning-facilitated synaptic plasticity occurs in the intermediate hippocampus in association with spatial learning. Front Synaptic Neurosci 5:10

    PubMed  PubMed Central  Google Scholar 

  • Kishi T, Tsumori T, Yokota S, Yasui Y (2006) Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J Comp Neurol 496(3):349–368

    PubMed  Google Scholar 

  • Lovinger DM (2002) NMDA receptors lose their inhibitions. Nat Neurosci 5(7):614–616

    CAS  PubMed  Google Scholar 

  • Lovinger DM, White G, Weight FF (1990) NMDA receptor-mediated synaptic excitation selectively inhibited by ethanol in hippocampal slice from adult rat. J Neurosci 10(4):1372–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu CB, Jefferys JGR, Toescu EC, Vreugdenhil M (2011) In vitro hippocampal gamma oscillation power as an index of in vivo CA3 gamma oscillation strength and spatial reference memory. Neurobiol Learn Mem 95(3):221–230

    PubMed  Google Scholar 

  • Matta R, Tiessen A, Choleris E (2017) The role of dorsal hippocampal dopamine D1-type receptors in social learning, social interactions, and food intake in male and female mice. Neuropsychopharmacology 42(12):2344–2353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matthews DB, Silvers JR (2004) The use of acute ethanol administration as a tool to investigate multiple memory systems. Neurobiol Learn Mem 82(3):299–308

    CAS  PubMed  Google Scholar 

  • Moonat S, Starkman BG, Sakharkar A, Pandey SC (2010) Neuroscience of alcoholism: molecular and cellular mechanisms. Cell Mol Life Sci 67(1):73–88

    CAS  PubMed  Google Scholar 

  • Moselhy HF, Georgiou G, Kahn A (2001) Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol 36(5):357–368

    CAS  PubMed  Google Scholar 

  • Pandis C, Sotiriou E, Kouvaras E, Asprodini E, Papatheodoropoulos C, Angelatou F (2006) Differential expression of NMDA and AMPA receptor subunits in rat dorsal and ventral hippocampus. Neuroscience 140(1):163–175

    CAS  PubMed  Google Scholar 

  • Petrovich GD, Canteras NS, Swanson LW (2001) Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 38(1–2):247–289

    CAS  PubMed  Google Scholar 

  • Pitkanen A et al (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391

    CAS  PubMed  Google Scholar 

  • Proctor WR, Diao L, Freund RK, Browning MD, Wu PH (2006) Synaptic GABAergic and glutamatergic mechanisms underlying alcohol sensitivity in mouse hippocampal neurons. J Physiol 575(Pt 1):145–159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rabin RA, Edelman AM, Wagner JA (1992) Activation of protein kinase A is necessary but not sufficient for ethanol-induced desensitization of cyclic AMP production. J Pharmacol Exp Ther 262(1):257–262

    CAS  PubMed  Google Scholar 

  • Risold PY, Thompson RH, Swanson LW (1997) The structural organization of connections between hypothalamus and cerebral cortex. Brain Res Brain Res Rev 24(2–3):197–254

    CAS  PubMed  Google Scholar 

  • Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207

    CAS  PubMed  Google Scholar 

  • Traub RD, Bibbig A, LeBeau FEN, Buhl EH, Whittington MA (2004) Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. Annu Rev Neurosci 27:247–278

    CAS  PubMed  Google Scholar 

  • Van Groen T, Wyss JM (2003) Connections of the retrosplenial granular b cortex in the rat. J Comp Neurol 463(3):249–263

    PubMed  Google Scholar 

  • Wang J et al (2016) Acute ethanol inhibition of γ oscillations is mediated by Akt and GSK3β. Front Cell Neurosci 10:189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bahner F, Both M, Tort ABL, Kopell NJ, Wisden W, Monyer H (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 106(9):3561–3566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu M, Woodward JJ (2006) Ethanol inhibition of NMDA receptors under conditions of altered protein kinase a activity. J Neurochem 96(6):1760–1767

    CAS  PubMed  Google Scholar 

  • Zeng T, Zhang CL, Song FY, Zhao XL, Yu LH, Zhu ZP, Xie KQ (2012) PI3K/Akt pathway activation was involved in acute ethanol-induced fatty liver in mice. Toxicology 296(1):56–66

    CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (NSFC, grant numbers: 81271422; U1804170; 81100953; 1070938), International Collaboration of Henan Province Science-Technique Bureau (134300510040), Natural Science Foundation of Hebei Province (H2012203067) and Key Program for Applied Basic Research of Hebei Key Program for Applied Basic Research of Hebei Province (12966119D).

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Contributions

ZRL and LCB designed and supervised the experiments; LZH, YB, and GFL performed the experiments; RF, ZHX, ZXY, LZH, and LCB analyzed the data. LCB, LZH, and ZRL wrote and revised the manuscript; All authors reviewed the manuscript.

Corresponding authors

Correspondence to Chengbiao Lu or Ruiling Zhang.

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On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Liu, Z., Ren, F., Yang, B. et al. Region-dependent regulation of acute ethanol on γ oscillation in the rat hippocampal slices. Psychopharmacology 237, 2959–2966 (2020). https://doi.org/10.1007/s00213-020-05584-y

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  • DOI: https://doi.org/10.1007/s00213-020-05584-y

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