[{"year":"2017","has_accepted_license":"1","isi":1,"publication":"Neuron","day":"18","page":"308 - 314","date_created":"2018-12-11T11:50:15Z","doi":"10.1016/j.neuron.2016.12.018","date_published":"2017-01-18T00:00:00Z","oa":1,"quality_controlled":"1","publisher":"Elsevier","citation":{"mla":"Gan, Jian, et al. “Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal Ripple Oscillations in Awake Mice in Vivo.” Neuron, vol. 93, no. 2, Elsevier, 2017, pp. 308–14, doi:10.1016/j.neuron.2016.12.018.","ama":"Gan J, Weng S-M, Pernia-Andrade A, Csicsvari JL, Jonas PM. Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo. Neuron. 2017;93(2):308-314. doi:10.1016/j.neuron.2016.12.018","apa":"Gan, J., Weng, S.-M., Pernia-Andrade, A., Csicsvari, J. L., & Jonas, P. M. (2017). Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo. Neuron. Elsevier. https://doi.org/10.1016/j.neuron.2016.12.018","ieee":"J. Gan, S.-M. Weng, A. Pernia-Andrade, J. L. Csicsvari, and P. M. Jonas, “Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo,” Neuron, vol. 93, no. 2. Elsevier, pp. 308–314, 2017.","short":"J. Gan, S.-M. Weng, A. Pernia-Andrade, J.L. Csicsvari, P.M. Jonas, Neuron 93 (2017) 308–314.","chicago":"Gan, Jian, Shih-Ming Weng, Alejandro Pernia-Andrade, Jozsef L Csicsvari, and Peter M Jonas. “Phase-Locked Inhibition, but Not Excitation, Underlies Hippocampal Ripple Oscillations in Awake Mice in Vivo.” Neuron. Elsevier, 2017. https://doi.org/10.1016/j.neuron.2016.12.018.","ista":"Gan J, Weng S-M, Pernia-Andrade A, Csicsvari JL, Jonas PM. 2017. Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo. Neuron. 93(2), 308–314."},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","article_processing_charge":"No","external_id":{"isi":["000396428200010"]},"publist_id":"6244","author":[{"id":"3614E438-F248-11E8-B48F-1D18A9856A87","first_name":"Jian","full_name":"Gan, Jian","last_name":"Gan"},{"id":"2F9C5AC8-F248-11E8-B48F-1D18A9856A87","first_name":"Shih-Ming","full_name":"Weng, Shih-Ming","last_name":"Weng"},{"full_name":"Pernia-Andrade, Alejandro","last_name":"Pernia-Andrade","id":"36963E98-F248-11E8-B48F-1D18A9856A87","first_name":"Alejandro"},{"id":"3FA14672-F248-11E8-B48F-1D18A9856A87","first_name":"Jozsef L","orcid":"0000-0002-5193-4036","full_name":"Csicsvari, Jozsef L","last_name":"Csicsvari"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","first_name":"Peter M","orcid":"0000-0001-5001-4804","full_name":"Jonas, Peter M","last_name":"Jonas"}],"title":"Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo","project":[{"name":"Mechanisms of transmitter release at GABAergic synapses","grant_number":"P24909-B24","_id":"25C26B1E-B435-11E9-9278-68D0E5697425","call_identifier":"FWF"},{"name":"Nanophysiology of fast-spiking, parvalbumin-expressing GABAergic interneurons","grant_number":"268548","_id":"25C0F108-B435-11E9-9278-68D0E5697425","call_identifier":"FP7"}],"publication_status":"published","language":[{"iso":"eng"}],"file":[{"date_created":"2018-12-12T10:08:56Z","file_name":"IST-2017-752-v1+1_1-s2.0-S0896627316309606-main.pdf","date_updated":"2018-12-12T10:08:56Z","file_size":2738950,"creator":"system","file_id":"4719","content_type":"application/pdf","access_level":"open_access","relation":"main_file"}],"ec_funded":1,"volume":93,"issue":"2","acknowledged_ssus":[{"_id":"M-Shop"},{"_id":"ScienComp"},{"_id":"PreCl"}],"abstract":[{"lang":"eng","text":"Sharp wave-ripple (SWR) oscillations play a key role in memory consolidation during non-rapid eye movement sleep, immobility, and consummatory behavior. However, whether temporally modulated synaptic excitation or inhibition underlies the ripples is controversial. To address this question, we performed simultaneous recordings of excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) and local field potentials (LFPs) in the CA1 region of awake mice in vivo. During SWRs, inhibition dominated over excitation, with a peak conductance ratio of 4.1 ± 0.5. Furthermore, the amplitude of SWR-associated IPSCs was positively correlated with SWR magnitude, whereas that of EPSCs was not. Finally, phase analysis indicated that IPSCs were phase-locked to individual ripple cycles, whereas EPSCs were uniformly distributed in phase space. Optogenetic inhibition indicated that PV+ interneurons provided a major contribution to SWR-associated IPSCs. Thus, phasic inhibition, but not excitation, shapes SWR oscillations in the hippocampal CA1 region in vivo."}],"oa_version":"Published Version","scopus_import":"1","intvolume":" 93","month":"01","date_updated":"2023-09-20T11:31:48Z","ddc":["571"],"file_date_updated":"2018-12-12T10:08:56Z","department":[{"_id":"PeJo"},{"_id":"JoCs"}],"_id":"1118","tmp":{"legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","short":"CC BY (4.0)"},"type":"journal_article","pubrep_id":"752","status":"public"},{"article_processing_charge":"No","publist_id":"5550","author":[{"last_name":"Kowalski","full_name":"Kowalski, Janina","id":"3F3CA136-F248-11E8-B48F-1D18A9856A87","first_name":"Janina"},{"id":"3614E438-F248-11E8-B48F-1D18A9856A87","first_name":"Jian","last_name":"Gan","full_name":"Gan, Jian"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","first_name":"Peter M","last_name":"Jonas","orcid":"0000-0001-5001-4804","full_name":"Jonas, Peter M"},{"id":"36963E98-F248-11E8-B48F-1D18A9856A87","first_name":"Alejandro","full_name":"Pernia-Andrade, Alejandro","last_name":"Pernia-Andrade"}],"title":"Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats","citation":{"ista":"Kowalski J, Gan J, Jonas PM, Pernia-Andrade A. 2016. Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats. Hippocampus. 26(5), 668–682.","chicago":"Kowalski, Janina, Jian Gan, Peter M Jonas, and Alejandro Pernia-Andrade. “Intrinsic Membrane Properties Determine Hippocampal Differential Firing Pattern in Vivo in Anesthetized Rats.” Hippocampus. Wiley, 2016. https://doi.org/10.1002/hipo.22550.","apa":"Kowalski, J., Gan, J., Jonas, P. M., & Pernia-Andrade, A. (2016). Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats. Hippocampus. Wiley. https://doi.org/10.1002/hipo.22550","ama":"Kowalski J, Gan J, Jonas PM, Pernia-Andrade A. Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats. Hippocampus. 2016;26(5):668-682. doi:10.1002/hipo.22550","short":"J. Kowalski, J. Gan, P.M. Jonas, A. Pernia-Andrade, Hippocampus 26 (2016) 668–682.","ieee":"J. Kowalski, J. Gan, P. M. Jonas, and A. Pernia-Andrade, “Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats,” Hippocampus, vol. 26, no. 5. Wiley, pp. 668–682, 2016.","mla":"Kowalski, Janina, et al. “Intrinsic Membrane Properties Determine Hippocampal Differential Firing Pattern in Vivo in Anesthetized Rats.” Hippocampus, vol. 26, no. 5, Wiley, 2016, pp. 668–82, doi:10.1002/hipo.22550."},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"quality_controlled":"1","publisher":"Wiley","acknowledgement":"The authors thank Jose Guzman for critically reading prior versions of the manuscript. They also thank T. Asenov for\r\nengineering mechanical devices, A. Schlögl for efficient pro-gramming, F. Marr for technical assistance, and E. Kramberger for manuscript editing.","page":"668 - 682","date_created":"2018-12-11T11:53:03Z","doi":"10.1002/hipo.22550","date_published":"2016-05-01T00:00:00Z","year":"2016","has_accepted_license":"1","publication":"Hippocampus","day":"01","tmp":{"short":"CC BY-NC-ND (4.0)","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","image":"/images/cc_by_nc_nd.png"},"type":"journal_article","pubrep_id":"469","status":"public","_id":"1616","department":[{"_id":"PeJo"}],"file_date_updated":"2020-07-14T12:45:07Z","date_updated":"2023-10-17T10:02:02Z","ddc":["570"],"scopus_import":"1","intvolume":" 26","month":"05","abstract":[{"text":"The hippocampus plays a key role in learning and memory. Previous studies suggested that the main types of principal neurons, dentate gyrus granule cells (GCs), CA3 pyramidal neurons, and CA1 pyramidal neurons, differ in their activity pattern, with sparse firing in GCs and more frequent firing in CA3 and CA1 pyramidal neurons. It has been assumed but never shown that such different activity may be caused by differential synaptic excitation. To test this hypothesis, we performed high-resolution whole-cell patch-clamp recordings in anesthetized rats in vivo. In contrast to previous in vitro data, both CA3 and CA1 pyramidal neurons fired action potentials spontaneously, with a frequency of ∼3–6 Hz, whereas GCs were silent. Furthermore, both CA3 and CA1 cells primarily fired in bursts. To determine the underlying mechanisms, we quantitatively assessed the frequency of spontaneous excitatory synaptic input, the passive membrane properties, and the active membrane characteristics. Surprisingly, GCs showed comparable synaptic excitation to CA3 and CA1 cells and the highest ratio of excitation versus hyperpolarizing inhibition. Thus, differential synaptic excitation is not responsible for differences in firing. Moreover, the three types of hippocampal neurons markedly differed in their passive properties. While GCs showed the most negative membrane potential, CA3 pyramidal neurons had the highest input resistance and the slowest membrane time constant. The three types of neurons also differed in the active membrane characteristics. GCs showed the highest action potential threshold, but displayed the largest gain of the input-output curves. In conclusion, our results reveal that differential firing of the three main types of hippocampal principal neurons in vivo is not primarily caused by differences in the characteristics of the synaptic input, but by the distinct properties of synaptic integration and input-output transformation.","lang":"eng"}],"oa_version":"Published Version","volume":26,"issue":"5","publication_status":"published","publication_identifier":{"eissn":["1098-1063"],"issn":["1050-9631"]},"language":[{"iso":"eng"}],"file":[{"checksum":"284b72b12fbe15474833ed3d4549f86b","file_id":"5033","access_level":"open_access","relation":"main_file","content_type":"application/pdf","date_created":"2018-12-12T10:13:47Z","file_name":"IST-2016-469-v1+1_Kowalski_et_al-Hippocampus.pdf","creator":"system","date_updated":"2020-07-14T12:45:07Z","file_size":905348}]},{"quality_controlled":"1","publisher":"American Association for the Advancement of Science","oa":1,"doi":"10.1126/science.1255263","date_published":"2014-08-01T00:00:00Z","date_created":"2018-12-11T11:55:29Z","has_accepted_license":"1","year":"2014","day":"01","publication":"Science","project":[{"_id":"25C26B1E-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Mechanisms of transmitter release at GABAergic synapses","grant_number":"P24909-B24"},{"_id":"25C0F108-B435-11E9-9278-68D0E5697425","call_identifier":"FP7","name":"Nanophysiology of fast-spiking, parvalbumin-expressing GABAergic interneurons","grant_number":"268548"}],"article_number":"1255263","publist_id":"4984","author":[{"last_name":"Hu","full_name":"Hu, Hua","id":"4AC0145C-F248-11E8-B48F-1D18A9856A87","first_name":"Hua"},{"full_name":"Gan, Jian","last_name":"Gan","id":"3614E438-F248-11E8-B48F-1D18A9856A87","first_name":"Jian"},{"orcid":"0000-0001-5001-4804","full_name":"Jonas, Peter M","last_name":"Jonas","first_name":"Peter M","id":"353C1B58-F248-11E8-B48F-1D18A9856A87"}],"title":"Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to microcircuit function","citation":{"ieee":"H. Hu, J. Gan, and P. M. Jonas, “Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to microcircuit function,” Science, vol. 345, no. 6196. American Association for the Advancement of Science, 2014.","short":"H. Hu, J. Gan, P.M. Jonas, Science 345 (2014).","apa":"Hu, H., Gan, J., & Jonas, P. M. (2014). Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to microcircuit function. Science. American Association for the Advancement of Science. https://doi.org/10.1126/science.1255263","ama":"Hu H, Gan J, Jonas PM. Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to microcircuit function. Science. 2014;345(6196). doi:10.1126/science.1255263","mla":"Hu, Hua, et al. “Fast-Spiking Parvalbumin^+ GABAergic Interneurons: From Cellular Design to Microcircuit Function.” Science, vol. 345, no. 6196, 1255263, American Association for the Advancement of Science, 2014, doi:10.1126/science.1255263.","ista":"Hu H, Gan J, Jonas PM. 2014. Fast-spiking parvalbumin^+ GABAergic interneurons: From cellular design to microcircuit function. Science. 345(6196), 1255263.","chicago":"Hu, Hua, Jian Gan, and Peter M Jonas. “Fast-Spiking Parvalbumin^+ GABAergic Interneurons: From Cellular Design to Microcircuit Function.” Science. American Association for the Advancement of Science, 2014. https://doi.org/10.1126/science.1255263."},"user_id":"4435EBFC-F248-11E8-B48F-1D18A9856A87","scopus_import":1,"month":"08","intvolume":" 345","abstract":[{"text":"The success story of fast-spiking, parvalbumin-positive (PV+) GABAergic interneurons (GABA, γ-aminobutyric acid) in the mammalian central nervous system is noteworthy. In 1995, the properties of these interneurons were completely unknown. Twenty years later, thanks to the massive use of subcellular patch-clamp techniques, simultaneous multiple-cell recording, optogenetics, in vivo measurements, and computational approaches, our knowledge about PV+ interneurons became more extensive than for several types of pyramidal neurons. These findings have implications beyond the “small world” of basic research on GABAergic cells. For example, the results provide a first proof of principle that neuroscientists might be able to close the gaps between the molecular, cellular, network, and behavioral levels, representing one of the main challenges at the present time. Furthermore, the results may form the basis for PV+ interneurons as therapeutic targets for brain disease in the future. However, much needs to be learned about the basic function of these interneurons before clinical neuroscientists will be able to use PV+ interneurons for therapeutic purposes.","lang":"eng"}],"oa_version":"Submitted Version","issue":"6196","volume":345,"ec_funded":1,"publication_status":"published","file":[{"file_id":"5185","checksum":"a0036a589037d37e86364fa25cc0a82f","relation":"main_file","access_level":"open_access","content_type":"application/pdf","file_name":"IST-2017-821-v1+1_1255263JonasPVReviewTextR_Final.pdf","date_created":"2018-12-12T10:16:00Z","creator":"system","file_size":215514,"date_updated":"2020-07-14T12:45:27Z"},{"checksum":"e1f57d2713725449cb898fdcb8ef47b8","file_id":"5186","content_type":"application/pdf","access_level":"open_access","relation":"main_file","date_created":"2018-12-12T10:16:01Z","file_name":"IST-2017-821-v1+2_1255263JonasPVReviewFigures_Final.pdf","date_updated":"2020-07-14T12:45:27Z","file_size":1732723,"creator":"system"}],"language":[{"iso":"eng"}],"type":"journal_article","status":"public","pubrep_id":"821","_id":"2062","file_date_updated":"2020-07-14T12:45:27Z","department":[{"_id":"PeJo"}],"date_updated":"2021-01-12T06:55:03Z","ddc":["570"]}]