Abstract
Aim:
To examine whether co-activation of nAChR and mGluR1 induced γ oscillation (20–60 Hz) in rat medial septum diagonal band of Broca (MSDB) slices.
Methods:
Rat brain sagittal slices containing the MSDB were prepared. Extracellular field potentials were recorded with glass microelectrodes. The nAChR and mGluR1 agonists were applied to the slices to induce network activity. Data analysis was performed off-line using software Spike 2.
Results:
Co-application of the nAChR agonist nicotine (1 μmol/L) and the mGluR1 agonist dihydroxyphenylglycine (DHPG, 25 μmol/L) was able to induce γ oscillation in MSDB slices. The intensity of nAChR and mGluR1 activation was critical for induction of network oscillation at a low (θ oscillation) or high frequency (γ oscillation): co-application of low concentrations of the two agonists only increased the power and frequency of oscillation within the range of θ, whereas γ oscillation mostly appeared when high concentrations of the two agonists were applied.
Conclusion:
Activation of mGluR1 and nAChR is able to program slow or fast network oscillation by altering the intensity of receptor activation, which may provide a mechanism for modulation of learning and memory.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA . Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 2010; 464: 763–7.
Kunec S, Hasselmo ME, Kopell N . Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. J Neurophysiol 2005; 94: 70–82.
Wyble BP, Hyman JM, Rossi CA, Hasselmo ME . Analysis of theta power in hippocampal EEG during bar pressing and running behavior in rats during distinct behavioral contexts. Hippocampus 2004; 14: 662–74.
Colom LV . Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease. J Neurochem 2006; 96: 609–23.
Tóth K, Freund TF, Miles R . Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol 1997; 500: 463–74.
Bland BH, Oddie SD, Colom LV, Vertes RP . Extrinsic modulation of medial septal cell discharges by the ascending brainstem hippocampal synchronizing pathway. Hippocampus 1994; 4: 649–60.
Kiss J, Kocsis K, Csáki A, Görcs TJ, Halász B . Metabotropic glutamate receptor in GHRH and beta-endorphin neurones of the hypothalamic arcuate nucleus. Neuroreport 1997; 8: 3703–7.
Izquierdo I, da Cunha C, Rosat R, Jerusalinsky D, Ferreira MB, Medina JH . Neurotransmitter receptors involved in post-training memory processing by the amygdala, medial septum, and hippocampus of the rat. Behav Neural Biol 1992; 58: 16–26.
Izquierdo I . Pharmacological evidence for a role of long-term potentiation in memory. FASEB J 1994; 8: 1139–45.
Vreugdenhil M, Toescu EC . Age-dependent reduction of gamma oscillations in the mouse hippocampus in vitro. Neuroscience 2005; 132: 1151–7.
Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ . Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 2004; 24: 9658–68.
Lu CB, Ouyang G, Henderson Z, Li X . Induction of theta-frequency oscillations in the rat medial septal diagonal band slice by metabotropic glutamate receptor agonists. Neuroscience 2011; 177: 1–11.
Garner HL, Whittington MA, Henderson Z . Induction by kainate of theta frequency rhythmic activity in the rat medial septum-diagonal band complex in vitro. J Physiol 2005; 564: 83–102.
Yakel JL . Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. Nicotine Tob Res 2012; 14: 1249–57.
Lu CB, Li CZ, Li DL, Henderson Z . Nicotine induction of theta frequency oscillations in rodent medial septal diagonal band in vitro. Acta Pharmacol Sin 2013; 34: 819–29.
Lu CB, Henderson Z . Nicotine induction of theta frequency oscillations in rodent hippocampus in vitro. Neuroscience 2010; 166: 84–93.
Song C, Murray TA, Kimura R, Wakui M, Ellsworth K, Javedan SP, et al. Role of alpha7-nicotinic acetylcholine receptors in tetanic stimulation–induced gamma oscillations in rat hippocampal slices. Neuropharmacology 2005; 48: 869–80.
Klein RC, Yakel JL . Inhibition of nicotinic acetylcholine receptors by apolipoprotein E-derived peptides in rat hippocampal slices. Neuroscience 2004; 127: 563–7.
Andersson R, Lindskog M, Fisahn A . Histamine H3 receptor activation decreases kainate-induced hippocampal gamma oscillations in vitro by action potential desynchronization in pyramidal neurons. J Physiol 2010; 588: 1241–9.
Jensen O, Kaiser J, Lachaux JP . Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 2007; 30: 317–24.
Hwang EJ, Andersen RA . Effects of visual stimulation on LFPs, spikes, and LFP-spike relations in PRR. J Neurophysiol 2011; 105: 1850–60.
Traub RD, Pais I, Bibbig A, Lebeau FE, Buhl EH, Garner H, et al. Transient depression of excitatory synapses on interneurons contributes to epileptiform bursts during gamma oscillations in the mouse hippocampal slice. J Neurophysiol 2005; 94: 1225–35.
Thinschmidt JS, Frazier CJ, King MA, Meyer EM, Papke RL . Medial septal/diagonal band cells express multiple functional nicotinic receptor subtypes that are correlated with firing frequency. Neurosci Lett 2005; 389: 163–8.
Lu CB, Li CZ, Li DL, Henderson Z . Nicotine induction of theta frequency oscillations in rodent medial septal diagonal band in vitro. Acta Pharmacol Sin 2013; 34: 819–29.
Fisahn A, Pike FG, Buhl EH, Paulsen O . Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 1998; 394: 186–9.
Traub RD, Bibbig A, LeBeau FE, Cunningham MO, Whittington MA . Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model. J Physiol 2005; 562: 3–8.
Pálhalmi J, Paulsen O, Freund TF, Hájos N . Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 2004; 47: 381–9.
Bartos M, Vida I, Jonas P . Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 2007; 8: 45–56.
Mann EO, Radcliffe CA, Paulsen O . Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back. J Physiol 2005; 562: 55–63.
Banks MI, White JA, Pearce RA . Interactions between distinct GABA(A) circuits in hippocampus. Neuron 2000; 25: 449–57.
Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JG . Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 1996; 493: 471–84.
Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH . Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 2000; 38: 315–36.
Rotstein HG, Pervouchine DD, Acker CD, Gillies MJ, White JA, Buhl EH, et al. Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. J Neurophysiol 2005; 94: 1509–18.
Akkurt D, Akay YM, Akay M . Investigating the synchronization of hippocampal neural network in response to acute nicotine exposure. J Neuroeng Rehabil 2010; 7: 31.
Phillips JM, Ehrlichman RS, Siegel SJ . Mecamylamine blocks nicotine-induced enhancement of the P20 auditory event-related potential and evoked gamma. Neuroscience 2007; 144: 1314–23.
Crawford HJ, McClain-Furmanski D, Castagnoli N Jr, Castagnoli K . Enhancement of auditory sensory gating and stimulus-bound gamma band (40 Hz) oscillations in heavy tobacco smokers. Neurosci Lett 2002; 317: 151–5.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (No 31070938; 81271422); the open project of the National Key Laboratory of Cognitive Neuroscience and Learning in Beijing Normal University and National Natural Science Funds for Distinguished Young Scholar (No 61025019). International Science and technology cooperation projects of Henan Province(2012);Scientific Reserch Fund of Xinxinag Medical University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, Yl., Wang, Jg., Ou-yang, Gx. et al. Co-activation of nAChR and mGluR induces γ oscillation in rat medial septum diagonal band of Broca slices. Acta Pharmacol Sin 35, 175–184 (2014). https://doi.org/10.1038/aps.2013.138
Received:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/aps.2013.138
