[{"page":"97","ddc":["570"],"alternative_title":["ISTA Thesis"],"article_processing_charge":"No","doi":"10.15479/AT:ISTA:6849","publisher":"Institute of Science and Technology Austria","_id":"6849","date_updated":"2023-09-19T10:01:12Z","type":"dissertation","degree_awarded":"PhD","status":"public","date_published":"2019-09-09T00:00:00Z","year":"2019","related_material":{"record":[{"id":"5914","status":"public","relation":"part_of_dissertation"}]},"has_accepted_license":"1","acknowledged_ssus":[{"_id":"Bio"},{"_id":"PreCl"},{"_id":"M-Shop"}],"abstract":[{"lang":"eng","text":"Brain function is mediated by complex dynamical interactions between excitatory and inhibitory cell types. The Cholecystokinin-expressing inhibitory cells (CCK-interneurons) are one of the least studied types, despite being suspected to play important roles in cognitive processes. We studied the network effects of optogenetic silencing of CCK-interneurons in the CA1 hippocampal area during exploration and sleep states. The cell firing pattern in response to light pulses allowed us to classify the recorded neurons in 5 classes, including disinhibited and non-responsive pyramidal cell and interneurons, and the inhibited interneurons corresponding to the CCK group. The light application, which inhibited the activity of CCK interneurons triggered wider changes in the firing dynamics of cells. We observed rate changes (i.e. remapping) of pyramidal cells during the exploration session in which the light was applied relative to the previous control session that was not restricted neither in time nor space to the light delivery. Also, the disinhibited pyramidal cells had higher increase in bursting than in single spike firing rate as a result of CCK silencing. In addition, the firing activity patterns during exploratory periods were more weakly reactivated in sleep for those periods in which CCK-interneuron were silenced than in the unaffected periods. Furthermore, light pulses during sleep disrupted the reactivation of recent waking patterns. Hence, silencing CCK neurons during exploration suppressed the reactivation of waking firing patterns in sleep and CCK interneuron activity was also required during sleep for the normal reactivation of waking patterns. These findings demonstrate the involvement of CCK cells in reactivation-related memory consolidation. An important part of our analysis was to test the relationship of the identified CCKinterneurons to brain oscillations. Our findings showed that these cells exhibited different oscillatory behaviour during anaesthesia and natural waking and sleep conditions. We showed that: 1) Contrary to the past studies performed under anaesthesia, the identified CCKinterneurons fired on the descending portion of the theta phase in waking exploration. 2) CCKinterneuron preferred phases around the trough of gamma oscillations. 3) Contrary to anaesthesia conditions, the average firing rate of the CCK-interneurons increased around the peak activity of the sharp-wave ripple (SWR) events in natural sleep, which is congruent with new reports about their functional connectivity. We also found that light driven CCK-interneuron silencing altered the dynamics on the CA1 network oscillatory activity: 1) Pyramidal cells negatively shifted their preferred theta phases when the light was applied, while interneurons responses were less consistent. 2) As a population, pyramidal cells negatively shifted their preferred activity during gamma oscillations, albeit we did not find gamma modulation differences related to the light application when pyramidal cells were subdivided into the disinhibited and unaffected groups. 3) During the peak of SWR events, all but the CCK-interneurons had a reduction in their relative firing rate change during the light application as compared to the change observed at SWR initiation. Finally, regarding to the place field activity of the recorded pyramidal neurons, we showed that the disinhibited pyramidal cells had reduced place field similarity, coherence and spatial information, but only during the light application. The mechanisms behind such observed behaviours might involve eCB signalling and plastic changes in CCK-interneuron synapses. In conclusion, the observed changes related to the light-mediated silencing of CCKinterneurons have unravelled characteristics of this interneuron subpopulation that might change the understanding not only of their particular network interactions, but also of the current theories about the emergence of certain cognitive processes such as place coding needed for navigation or hippocampus-dependent memory consolidation. "}],"file_date_updated":"2021-02-10T23:30:09Z","publication_identifier":{"issn":["2663-337X"],"isbn":["9783990780039"]},"publication_status":"published","day":"09","author":[{"first_name":"Dámaris K","orcid":"0000-0002-8602-4374","last_name":"Rangel Guerrero","full_name":"Rangel Guerrero, Dámaris K","id":"4871BCE6-F248-11E8-B48F-1D18A9856A87"}],"oa_version":"Published Version","title":"The role of CCK-interneurons in regulating hippocampal network dynamics","date_created":"2019-09-06T06:54:16Z","oa":1,"language":[{"iso":"eng"}],"citation":{"chicago":"Rangel Guerrero, Dámaris K. “The Role of CCK-Interneurons in Regulating Hippocampal Network Dynamics.” Institute of Science and Technology Austria, 2019. <a href=\"https://doi.org/10.15479/AT:ISTA:6849\">https://doi.org/10.15479/AT:ISTA:6849</a>.","ista":"Rangel Guerrero DK. 2019. The role of CCK-interneurons in regulating hippocampal network dynamics. Institute of Science and Technology Austria.","apa":"Rangel Guerrero, D. K. (2019). <i>The role of CCK-interneurons in regulating hippocampal network dynamics</i>. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT:ISTA:6849\">https://doi.org/10.15479/AT:ISTA:6849</a>","mla":"Rangel Guerrero, Dámaris K. <i>The Role of CCK-Interneurons in Regulating Hippocampal Network Dynamics</i>. Institute of Science and Technology Austria, 2019, doi:<a href=\"https://doi.org/10.15479/AT:ISTA:6849\">10.15479/AT:ISTA:6849</a>.","ama":"Rangel Guerrero DK. The role of CCK-interneurons in regulating hippocampal network dynamics. 2019. doi:<a href=\"https://doi.org/10.15479/AT:ISTA:6849\">10.15479/AT:ISTA:6849</a>","ieee":"D. K. Rangel Guerrero, “The role of CCK-interneurons in regulating hippocampal network dynamics,” Institute of Science and Technology Austria, 2019.","short":"D.K. Rangel Guerrero, The Role of CCK-Interneurons in Regulating Hippocampal Network Dynamics, Institute of Science and Technology Austria, 2019."},"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","supervisor":[{"full_name":"Csicsvari, Jozsef L","id":"3FA14672-F248-11E8-B48F-1D18A9856A87","last_name":"Csicsvari","first_name":"Jozsef L","orcid":"0000-0002-5193-4036"}],"month":"09","department":[{"_id":"JoCs"}],"file":[{"creator":"drangel","date_updated":"2021-02-10T23:30:09Z","file_size":18253100,"date_created":"2019-09-09T13:09:45Z","embargo_to":"open_access","file_id":"6865","access_level":"closed","content_type":"application/vnd.openxmlformats-officedocument.wordprocessingml.document","file_name":"Thesis_Damaris_Rangel_source.docx","checksum":"244dc4f74dbfc94f414156092298831f","relation":"source_file"},{"file_id":"6866","embargo":"2020-09-10","date_updated":"2020-09-11T22:30:04Z","creator":"drangel","file_size":2160109,"date_created":"2019-09-09T13:09:52Z","request_a_copy":0,"checksum":"59c73be40eeaa1c4db24067270151555","relation":"main_file","content_type":"application/pdf","access_level":"open_access","file_name":"Thesis_Damaris_Rangel_pdfa.pdf"}]},{"language":[{"iso":"eng"}],"oa":1,"user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","citation":{"ama":"Rangel Guerrero DK, Donnett JG, Csicsvari JL, Kovács K. Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR events to learning. <i>eNeuro</i>. 2018;5(4). doi:<a href=\"https://doi.org/10.1523/ENEURO.0087-18.2018\">10.1523/ENEURO.0087-18.2018</a>","short":"D.K. Rangel Guerrero, J.G. Donnett, J.L. Csicsvari, K. Kovács, ENeuro 5 (2018).","ieee":"D. K. Rangel Guerrero, J. G. Donnett, J. L. Csicsvari, and K. Kovács, “Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR events to learning,” <i>eNeuro</i>, vol. 5, no. 4. Society of Neuroscience, 2018.","ista":"Rangel Guerrero DK, Donnett JG, Csicsvari JL, Kovács K. 2018. Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR events to learning. eNeuro. 5(4), e0087.","chicago":"Rangel Guerrero, Dámaris K, James G. Donnett, Jozsef L Csicsvari, and Krisztián Kovács. “Tetrode Recording from the Hippocampus of Behaving Mice Coupled with Four-Point-Irradiation Closed-Loop Optogenetics: A Technique to Study the Contribution of Hippocampal SWR Events to Learning.” <i>ENeuro</i>. Society of Neuroscience, 2018. <a href=\"https://doi.org/10.1523/ENEURO.0087-18.2018\">https://doi.org/10.1523/ENEURO.0087-18.2018</a>.","mla":"Rangel Guerrero, Dámaris K., et al. “Tetrode Recording from the Hippocampus of Behaving Mice Coupled with Four-Point-Irradiation Closed-Loop Optogenetics: A Technique to Study the Contribution of Hippocampal SWR Events to Learning.” <i>ENeuro</i>, vol. 5, no. 4, e0087, Society of Neuroscience, 2018, doi:<a href=\"https://doi.org/10.1523/ENEURO.0087-18.2018\">10.1523/ENEURO.0087-18.2018</a>.","apa":"Rangel Guerrero, D. K., Donnett, J. G., Csicsvari, J. L., &#38; Kovács, K. (2018). Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR events to learning. <i>ENeuro</i>. Society of Neuroscience. <a href=\"https://doi.org/10.1523/ENEURO.0087-18.2018\">https://doi.org/10.1523/ENEURO.0087-18.2018</a>"},"issue":"4","month":"07","file":[{"file_id":"5921","file_size":3746884,"date_created":"2019-02-05T12:48:36Z","date_updated":"2020-07-14T12:47:13Z","creator":"dernst","relation":"main_file","checksum":"f4915d45fc7ad4648b7b7a13fdecca01","file_name":"2018_ENeuro_Guerrero.pdf","access_level":"open_access","content_type":"application/pdf"}],"article_number":"e0087","department":[{"_id":"JoCs"}],"abstract":[{"lang":"eng","text":"With the advent of optogenetics, it became possible to change the activity of a targeted population of neurons in a temporally controlled manner. To combine the advantages of 60-channel in vivo tetrode recording and laser-based optogenetics, we have developed a closed-loop recording system that allows for the actual electrophysiological signal to be used as a trigger for the laser light mediating the optogenetic intervention. We have optimized the weight, size, and shape of the corresponding implant to make it compatible with the size, force, and movements of a behaving mouse, and we have shown that the system can efficiently block sharp wave ripple (SWR) events using those events themselves as a trigger. To demonstrate the full potential of the optogenetic recording system we present a pilot study addressing the contribution of SWR events to learning in a complex behavioral task."}],"tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"intvolume":"         5","has_accepted_license":"1","file_date_updated":"2020-07-14T12:47:13Z","publication_status":"published","oa_version":"Published Version","title":"Tetrode recording from the hippocampus of behaving mice coupled with four-point-irradiation closed-loop optogenetics: A technique to study the contribution of Hippocampal SWR events to learning","day":"27","scopus_import":"1","author":[{"last_name":"Rangel Guerrero","full_name":"Rangel Guerrero, Dámaris K","id":"4871BCE6-F248-11E8-B48F-1D18A9856A87","first_name":"Dámaris K","orcid":"0000-0002-8602-4374"},{"last_name":"Donnett","full_name":"Donnett, James G.","first_name":"James G."},{"full_name":"Csicsvari, Jozsef L","id":"3FA14672-F248-11E8-B48F-1D18A9856A87","last_name":"Csicsvari","orcid":"0000-0002-5193-4036","first_name":"Jozsef L"},{"orcid":"0000-0001-6251-1007","first_name":"Krisztián","last_name":"Kovács","full_name":"Kovács, Krisztián","id":"2AB5821E-F248-11E8-B48F-1D18A9856A87"}],"date_created":"2019-02-03T22:59:16Z","volume":5,"publication":"eNeuro","status":"public","project":[{"_id":"25681D80-B435-11E9-9278-68D0E5697425","call_identifier":"FP7","name":"International IST Postdoc Fellowship Programme","grant_number":"291734"},{"_id":"257D4372-B435-11E9-9278-68D0E5697425","name":"Interneuron plasticity during spatial learning","grant_number":"I2072-B27","call_identifier":"FWF"}],"date_published":"2018-07-27T00:00:00Z","ec_funded":1,"related_material":{"record":[{"id":"6849","status":"public","relation":"dissertation_contains"}]},"external_id":{"isi":["000443994700007"]},"isi":1,"year":"2018","ddc":["570"],"quality_controlled":"1","publisher":"Society of Neuroscience","article_processing_charge":"No","doi":"10.1523/ENEURO.0087-18.2018","type":"journal_article","_id":"5914","date_updated":"2024-03-25T23:30:06Z"},{"oa":1,"pubrep_id":"690","language":[{"iso":"eng"}],"issue":"10","citation":{"chicago":"Kovács, Krisztián, Joseph O’Neill, Philipp Schönenberger, Markku Penttonen, Dámaris K Rangel Guerrero, and Jozsef L Csicsvari. “Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus.” <i>PLoS One</i>. Public Library of Science, 2016. <a href=\"https://doi.org/10.1371/journal.pone.0164675\">https://doi.org/10.1371/journal.pone.0164675</a>.","ista":"Kovács K, O’Neill J, Schönenberger P, Penttonen M, Rangel Guerrero DK, Csicsvari JL. 2016. Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus. PLoS One. 11(10), e0164675.","mla":"Kovács, Krisztián, et al. “Optogenetically Blocking Sharp Wave Ripple Events in Sleep Does Not Interfere with the Formation of Stable Spatial Representation in the CA1 Area of the Hippocampus.” <i>PLoS One</i>, vol. 11, no. 10, e0164675, Public Library of Science, 2016, doi:<a href=\"https://doi.org/10.1371/journal.pone.0164675\">10.1371/journal.pone.0164675</a>.","apa":"Kovács, K., O’Neill, J., Schönenberger, P., Penttonen, M., Rangel Guerrero, D. K., &#38; Csicsvari, J. L. (2016). Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus. <i>PLoS One</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pone.0164675\">https://doi.org/10.1371/journal.pone.0164675</a>","ama":"Kovács K, O’Neill J, Schönenberger P, Penttonen M, Rangel Guerrero DK, Csicsvari JL. Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus. <i>PLoS One</i>. 2016;11(10). doi:<a href=\"https://doi.org/10.1371/journal.pone.0164675\">10.1371/journal.pone.0164675</a>","short":"K. Kovács, J. O’Neill, P. Schönenberger, M. Penttonen, D.K. Rangel Guerrero, J.L. Csicsvari, PLoS One 11 (2016).","ieee":"K. Kovács, J. O’Neill, P. Schönenberger, M. Penttonen, D. K. Rangel Guerrero, and J. L. Csicsvari, “Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus,” <i>PLoS One</i>, vol. 11, no. 10. Public Library of Science, 2016."},"user_id":"3E5EF7F0-F248-11E8-B48F-1D18A9856A87","month":"10","department":[{"_id":"JoCs"}],"file":[{"checksum":"395895ecb2216e9c39135abaa56b28b3","relation":"main_file","content_type":"application/pdf","access_level":"open_access","file_name":"IST-2016-690-v1+1_journal.pone.0164675.PDF","file_id":"5009","date_updated":"2020-07-14T12:44:42Z","creator":"system","file_size":4353592,"date_created":"2018-12-12T10:13:26Z"}],"article_number":"e0164675","has_accepted_license":"1","tmp":{"name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","short":"CC BY (4.0)"},"abstract":[{"text":"During hippocampal sharp wave/ripple (SWR) events, previously occurring, sensory inputdriven neuronal firing patterns are replayed. Such replay is thought to be important for plasticity- related processes and consolidation of memory traces. It has previously been shown that the electrical stimulation-induced disruption of SWR events interferes with learning in rodents in different experimental paradigms. On the other hand, the cognitive map theory posits that the plastic changes of the firing of hippocampal place cells constitute the electrophysiological counterpart of the spatial learning, observable at the behavioral level. Therefore, we tested whether intact SWR events occurring during the sleep/rest session after the first exploration of a novel environment are needed for the stabilization of the CA1 code, which process requires plasticity. We found that the newly-formed representation in the CA1 has the same level of stability with optogenetic SWR blockade as with a control manipulation that delivered the same amount of light into the brain. Therefore our results suggest that at least in the case of passive exploratory behavior, SWR-related plasticity is dispensable for the stability of CA1 ensembles.","lang":"eng"}],"intvolume":"        11","publication_status":"published","file_date_updated":"2020-07-14T12:44:42Z","author":[{"full_name":"Kovács, Krisztián","id":"2AB5821E-F248-11E8-B48F-1D18A9856A87","last_name":"Kovács","first_name":"Krisztián"},{"last_name":"O'Neill","full_name":"O'Neill, Joseph","id":"426376DC-F248-11E8-B48F-1D18A9856A87","first_name":"Joseph"},{"first_name":"Philipp","id":"3B9D816C-F248-11E8-B48F-1D18A9856A87","full_name":"Schönenberger, Philipp","last_name":"Schönenberger"},{"first_name":"Markku","last_name":"Penttonen","full_name":"Penttonen, Markku"},{"orcid":"0000-0002-8602-4374","first_name":"Dámaris K","id":"4871BCE6-F248-11E8-B48F-1D18A9856A87","full_name":"Rangel Guerrero, Dámaris K","last_name":"Rangel Guerrero"},{"first_name":"Jozsef L","orcid":"0000-0002-5193-4036","id":"3FA14672-F248-11E8-B48F-1D18A9856A87","full_name":"Csicsvari, Jozsef L","last_name":"Csicsvari"}],"scopus_import":1,"day":"19","oa_version":"Published Version","title":"Optogenetically blocking sharp wave ripple events in sleep does not interfere with the formation of stable spatial representation in the CA1 area of the hippocampus","volume":11,"date_created":"2018-12-11T11:51:06Z","project":[{"_id":"25681D80-B435-11E9-9278-68D0E5697425","grant_number":"291734","name":"International IST Postdoc Fellowship Programme","call_identifier":"FP7"},{"call_identifier":"FP7","grant_number":"281511","name":"Memory-related information processing in neuronal circuits of the hippocampus and entorhinal cortex","_id":"257A4776-B435-11E9-9278-68D0E5697425"}],"status":"public","publication":"PLoS One","ec_funded":1,"date_published":"2016-10-19T00:00:00Z","acknowledgement":"The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union's Seventh Framework Programme (FP7/2007-2013) under REA grant agreement n° [291734] via the IST FELLOWSHIP awarded to Dr. Krisztián A. Kovács and the European Research Council starting grant (acronym: HIPECMEM Project reference: 281511) awarded to Dr. Jozsef Csicsvari. We thank Lauri Viljanto for technical help in building the ripple detector.","year":"2016","publist_id":"6037","ddc":["570","571"],"quality_controlled":"1","doi":"10.1371/journal.pone.0164675","publisher":"Public Library of Science","date_updated":"2021-01-12T06:49:35Z","_id":"1279","type":"journal_article"}]