Tresóné Takács, Virág and Cserép, Csaba and Schlingloff, Dániel and Pósfai, Balázs and Szőnyi, András and Sós, Katalin Eszter and Környei, Zsuzsanna and Dénes, Ádám and Gulyás, Attila and Freund, Tamás and Nyíri, Gábor (2018) Co-transmission of acetylcholine and GABA regulates hippocampal states. NATURE COMMUNICATIONS, 9 (1). ISSN 2041-1723
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Official URL: http://doi.org/10.1038/s41467-018-05136-1
Abstract
The basal forebrain cholinergic system is widely assumed to control cortical functions via non-synaptic transmission of a single neurotransmitter. Yet, we find that mouse hippocampal cholinergic terminals invariably establish GABAergic synapses, and their cholinergic vesicles dock at those synapses only. We demonstrate that these synapses do not co-release but co-transmit GABA and acetylcholine via different vesicles, whose release is triggered by distinct calcium channels. This co-transmission evokes composite postsynaptic potentials, which are mutually cross-regulated by presynaptic autoreceptors. Although postsynaptic cholinergic receptor distribution cannot be investigated, their response latencies suggest a focal, intra- and/or peri-synaptic localisation, while GABAA receptors are detected intra-synaptically. The GABAergic component alone effectively suppresses hippocampal sharp wave-ripples and epileptiform activity. Therefore, the differentially regulated GABAergic and cholinergic co-transmission suggests a hitherto unrecognised level of control over cortical states. This novel model of hippocampal cholinergic neurotransmission may lead to alternative pharmacotherapies after cholinergic deinnervation seen in neurodegenerative disorders.
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| Additional Information: | Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 12 March 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 24 April 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 29 April 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 13 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 15 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :15 Export Date: 18 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 23 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 24 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 25 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 26 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 29 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, 1085, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Momentum Laboratory of Neuroimmunology, Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43, Budapest, 1083, Hungary Cited By :16 Export Date: 30 May 2020 Correspondence Address: Nyiri, G.; Laboratory of Cerebral Cortex Research Institute of Experimental Medicine, Hungarian Academy of Sciences, Szigony u 43Hungary; email: nyiri@koki.hu Chemicals/CAS: 4 aminobutyric acid, 28805-76-7, 56-12-2; acetylcholine, 51-84-3, 60-31-1, 66-23-9; gephyrin, 147570-97-6; vesicular acetylcholine transporter, 158132-77-5; calcium, 7440-70-2, 14092-94-5; Acetylcholine; Calcium; gamma-Aminobutyric Acid; Neurotransmitter Agents; Receptors, GABA-A Funding details: National Institutes of Health, NIH, NS030549 Funding details: European Research Council, ERC, ERC-2011-ADG-294313 Funding details: Magyar Tudományos Akadémia, MTA, ERC-CoG 724994 Funding details: Hungarian Scientific Research Fund, OTKA, UNKP-16-2-13, K119521, K115441, KH124345, EU H2020 720270, VKSZ_14-1-2O15-0155 Funding details: KTIA_13_NAP-A-I/2 Funding text 1: This work was supported by the European Research Council (ERC-2011-ADG-294313, SERRACO), National Institutes of Health, USA (NS030549), National Research, Development and Innovation Office, Hungary (OTKA K119521, OTKA K115441, OTKA KH124345 and VKSZ_14-1-2O15-0155), Human Brain Project, EU (EU H2020 720270); B.P. is supported by UNKP-16-2-13 and D.S. is supported by the UNKP-16-3-IV New National Excellence Program of the Ministry of Human Capacities, Hungary. Á. D. is supported by the Hungarian Brain Research Program KTIA_13_NAP-A-I/2, the ‘Momentum’ Program of the Hungarian Academy of Sciences and ERC-CoG 724994. We thank László Barna, the Nikon Microscopy Center at IEM, Nikon Austria GmbH and Auro-Science Consulting Ltd for technical support for fluorescent and STORM imaging. We thank Emőke Szépné Simon, Katalin Lengyel, Katalin Iványi, Győző Goda and Nándor Kriczky for assistance, and Anna Jász for help in scripting. We thank Dr. David Mastronarde (Univ. of Colorado Boulder) for help with electron tomography software IMOD. We thank Drs László Acsády, Julian Budd, Balázs Hangya, and Liset Menendez de la Prida for their comment on an earlier version of the manuscript. |
| Subjects: | R Medicine / orvostudomány > RC Internal medicine / belgyógyászat > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry / idegkórtan, neurológia, pszichiátria |
| SWORD Depositor: | MTMT SWORD |
| Depositing User: | MTMT SWORD |
| Date Deposited: | 28 Sep 2020 13:15 |
| Last Modified: | 28 Sep 2020 13:15 |
| URI: | http://real.mtak.hu/id/eprint/115126 |
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