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Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models

Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in... Betterton et al. BMC Neuroscience 2015, 16(Suppl 1):P267 http://www.biomedcentral.com/1471-2202/16/S1/P267 POSTER PRESENTATION Open Access Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models 1* 1 2 Ruth Betterton , Jack Mellor , Krasimira Tsaneva-Atanasova From 24th Annual Computational Neuroscience Meeting: CNS*2015 Prague, Czech Republic. 18-23 July 2015 A neuronal oscillation involves the rhythmic, synchro- elicited robust synaptic responses in the CA3 and CA1 nous firing of a population of cells. Oscillations found regions that were blocked by the application of NBQX throughout the cortex can be separated into bands of (10 µM) or TTX (1 µM). Local field potential recordings differing frequencies which are associated with various showed that a 1s step optical stimulation induced low power and low frequency gamma oscillations which atte- behavioural states. Gamma oscillations (30 - 100 Hz) occur coincidently with attention, sensory processing nuated over time. In vivo, gamma oscillations are often and learning and memory. The hippocampus, known for found ‘nested’ within an overlying theta oscillation [8]. its role in learning and memory, shows gamma activity Correlating well with these in vivo recordings, theta fre- in vivo [1] and gamma oscillations can be induced in quency (5 Hz) sine wave optical stimulation induced in vitro slices [2]. The release of acetylcholine (ACh) higher power and higher frequency gamma oscillations correlates with increases in oscillatory power in vivo [3] with less attenuation over a 1s period. and knockout of specific ACh receptor subtypes pro- We introduced, a similar, 5 Hz sine depolarising input vides evidence for this scenario [4]. To further investi- to the pyramidal cells in our mathematical model and gate the role of ACh in the modulation of gamma found that it was able to induce oscillations at gamma oscillations we have utilised both in vitro and computa- frequency. tional techniques. By manipulating specific currents within the model, We implemented a mathematical model of the CA3 we predicted the effect of specific ACh receptor subtype region of the hippocampus based on [5]. Using Hodg- activation on gamma oscillations. These predictions kin-Huxley single compartmental neurons, we verify were supported by our in vitro experimental evidence that a network of 80 excitatory pyramidal cells and 20 showing that we found that activation of ACh receptors inhibitory interneurons is able to produce oscillatory did indeed modulate gamma oscillations with M1 recep- activity within the gamma range. tor having a major effect. We developed an optogenetic system (see [6,7]) to induce gamma oscillations enabling us to test modulation Authors’ details by specific acetylcholine receptors. Male mice received School of Physiology and Pharmacology, University of Bristol, Bristol, BS8 stereotaxic injection into the CA3 region of the hippocam- 1TD, UK. College of Engineering, Mathematics and Physical Sciences, University of Exeter, Exeter, EX4 4QF, UK. pus of a viral vector (AAV5) containing channelrhodopsin (hChR2(H134R)) under the control of the CaMKIIa pro- Published: 18 December 2015 moter. Stimulation of the ChR expressing CA3 pyramidal cell bodies with short light pulses (5-50 ms) evoked action References 1. Csicsvari J, Jamieson B, Wise KD, Buzsáki G: Mechanisms of gamma potentials and stimulation of Schaffer collateral axons oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322. 2. Pálhalmi J, Paulsen O, Freund TF, Hájos N: Distinct properties of carbachol- * Correspondence: r.betterton@bristol.ac.uk 1 and DHPG-induced network oscillations in hippocampal slices. School of Physiology and Pharmacology, University of Bristol, Bristol, BS8 Neuropharmacology 2004, 47:381-389. 1TD, UK Full list of author information is available at the end of the article © 2015 Betterton et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/ zero/1.0/) applies to the data made available in this article, unless otherwise stated. Betterton et al. BMC Neuroscience 2015, 16(Suppl 1):P267 Page 2 of 2 http://www.biomedcentral.com/1471-2202/16/S1/P267 3. Morrosu F, Portas C, Mascia MS, Casu MA, Fà M, Giagheddu M, Imperato A, Gessa GL: Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain research 1995, 671:329-332. 4. Fisahn A, Pike FG, Buhl E, Paulsen O: Cholinergic induction of network oscillations at 40Hz in the hippocampus in vitro. Nature 1998, 394:186-188. 5. Kopell N, Börgers C, Pervouchine D, Malerba P, Tort A: Gamma and Theta Rhythms in Biophysical Models of Hippocampal Circuits. Hippocampal Microcircuits, Springer Series in Computational Neuroscience 5 New York: Springer; 2010. 6. Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM: Oscillatory dynamics in the hippocampus support dentate gyrus-CA3 coupling. Nature Neuroscience 2012, 15(5):763-768. 7. Pastoll H, Solanka L, van Rossum MCW, Nolan MF: Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields. Neuron 2012, 77:141-154. 8. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser M, Moser EI: Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357. doi:10.1186/1471-2202-16-S1-P267 Cite this article as: Betterton et al.: Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models. BMC Neuroscience 2015 16(Suppl 1):P267. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Neuroscience Springer Journals

Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models

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Springer Journals
Copyright
Copyright © 2015 by Betterton et al.
Subject
Biomedicine; Neurosciences; Neurobiology; Animal Models
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1471-2202
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10.1186/1471-2202-16-S1-P267
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Abstract

Betterton et al. BMC Neuroscience 2015, 16(Suppl 1):P267 http://www.biomedcentral.com/1471-2202/16/S1/P267 POSTER PRESENTATION Open Access Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models 1* 1 2 Ruth Betterton , Jack Mellor , Krasimira Tsaneva-Atanasova From 24th Annual Computational Neuroscience Meeting: CNS*2015 Prague, Czech Republic. 18-23 July 2015 A neuronal oscillation involves the rhythmic, synchro- elicited robust synaptic responses in the CA3 and CA1 nous firing of a population of cells. Oscillations found regions that were blocked by the application of NBQX throughout the cortex can be separated into bands of (10 µM) or TTX (1 µM). Local field potential recordings differing frequencies which are associated with various showed that a 1s step optical stimulation induced low power and low frequency gamma oscillations which atte- behavioural states. Gamma oscillations (30 - 100 Hz) occur coincidently with attention, sensory processing nuated over time. In vivo, gamma oscillations are often and learning and memory. The hippocampus, known for found ‘nested’ within an overlying theta oscillation [8]. its role in learning and memory, shows gamma activity Correlating well with these in vivo recordings, theta fre- in vivo [1] and gamma oscillations can be induced in quency (5 Hz) sine wave optical stimulation induced in vitro slices [2]. The release of acetylcholine (ACh) higher power and higher frequency gamma oscillations correlates with increases in oscillatory power in vivo [3] with less attenuation over a 1s period. and knockout of specific ACh receptor subtypes pro- We introduced, a similar, 5 Hz sine depolarising input vides evidence for this scenario [4]. To further investi- to the pyramidal cells in our mathematical model and gate the role of ACh in the modulation of gamma found that it was able to induce oscillations at gamma oscillations we have utilised both in vitro and computa- frequency. tional techniques. By manipulating specific currents within the model, We implemented a mathematical model of the CA3 we predicted the effect of specific ACh receptor subtype region of the hippocampus based on [5]. Using Hodg- activation on gamma oscillations. These predictions kin-Huxley single compartmental neurons, we verify were supported by our in vitro experimental evidence that a network of 80 excitatory pyramidal cells and 20 showing that we found that activation of ACh receptors inhibitory interneurons is able to produce oscillatory did indeed modulate gamma oscillations with M1 recep- activity within the gamma range. tor having a major effect. We developed an optogenetic system (see [6,7]) to induce gamma oscillations enabling us to test modulation Authors’ details by specific acetylcholine receptors. Male mice received School of Physiology and Pharmacology, University of Bristol, Bristol, BS8 stereotaxic injection into the CA3 region of the hippocam- 1TD, UK. College of Engineering, Mathematics and Physical Sciences, University of Exeter, Exeter, EX4 4QF, UK. pus of a viral vector (AAV5) containing channelrhodopsin (hChR2(H134R)) under the control of the CaMKIIa pro- Published: 18 December 2015 moter. Stimulation of the ChR expressing CA3 pyramidal cell bodies with short light pulses (5-50 ms) evoked action References 1. Csicsvari J, Jamieson B, Wise KD, Buzsáki G: Mechanisms of gamma potentials and stimulation of Schaffer collateral axons oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322. 2. Pálhalmi J, Paulsen O, Freund TF, Hájos N: Distinct properties of carbachol- * Correspondence: r.betterton@bristol.ac.uk 1 and DHPG-induced network oscillations in hippocampal slices. School of Physiology and Pharmacology, University of Bristol, Bristol, BS8 Neuropharmacology 2004, 47:381-389. 1TD, UK Full list of author information is available at the end of the article © 2015 Betterton et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/ zero/1.0/) applies to the data made available in this article, unless otherwise stated. Betterton et al. BMC Neuroscience 2015, 16(Suppl 1):P267 Page 2 of 2 http://www.biomedcentral.com/1471-2202/16/S1/P267 3. Morrosu F, Portas C, Mascia MS, Casu MA, Fà M, Giagheddu M, Imperato A, Gessa GL: Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain research 1995, 671:329-332. 4. Fisahn A, Pike FG, Buhl E, Paulsen O: Cholinergic induction of network oscillations at 40Hz in the hippocampus in vitro. Nature 1998, 394:186-188. 5. Kopell N, Börgers C, Pervouchine D, Malerba P, Tort A: Gamma and Theta Rhythms in Biophysical Models of Hippocampal Circuits. Hippocampal Microcircuits, Springer Series in Computational Neuroscience 5 New York: Springer; 2010. 6. Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM: Oscillatory dynamics in the hippocampus support dentate gyrus-CA3 coupling. Nature Neuroscience 2012, 15(5):763-768. 7. Pastoll H, Solanka L, van Rossum MCW, Nolan MF: Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields. Neuron 2012, 77:141-154. 8. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser M, Moser EI: Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357. doi:10.1186/1471-2202-16-S1-P267 Cite this article as: Betterton et al.: Modulation of hippocampal gamma oscillations by acetylcholine: insights from mathematical and in vitro optogenetic models. BMC Neuroscience 2015 16(Suppl 1):P267. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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BMC Neuroscience – Springer Journals

Published: Dec 4, 2015

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