{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,7]],"date-time":"2026-05-07T04:07:14Z","timestamp":1778126834774,"version":"3.51.4"},"reference-count":71,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T00:00:00Z","timestamp":1616025600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004442","name":"Narodowym Centrum Nauki","doi-asserted-by":"publisher","award":["UMO-2016\/23\/B\/NZ\/03657"],"award-info":[{"award-number":["UMO-2016\/23\/B\/NZ\/03657"]}],"id":[{"id":"10.13039\/501100004442","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Welcome Trust","doi-asserted-by":"crossref","id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Wake-related ketamine-dependent high frequency oscillations (HFO) can be recorded in local field potentials (LFP) from cortical and subcortical regions in rodents. The mechanisms underlying their generation and occurrence in higher mammals are unclear. Unfortunately, anesthetic doses of pure ketamine attenuate HFO, which has precluded their investigation under anesthesia. Here, we show ketamine-xylazine (KX) anesthesia is associated with a prominent 80\u2013130 Hz rhythm in the olfactory bulb (OB) of rats, whereas 30\u201365 Hz gamma power is diminished. Simultaneous LFP and thermocouple recordings revealed the 80\u2013130 Hz rhythm was dependent on nasal respiration. This rhythm persisted despite surgical excision of the piriform cortex. Silicon probes spanning the dorsoventral aspect of the OB revealed this rhythm was strongest in ventral areas and associated with microcurrent sources about the mitral layer. Pharmacological microinfusion studies revealed dependency on excitatory-inhibitory synaptic activity, but not gap junctions. Finally, a similar rhythm occurred in the OB of KX-anesthetized cats, which shared key features with our rodent studies. We conclude that the activity we report here is driven by nasal airflow, local excitatory-inhibitory interactions, and conserved in higher mammals. Additionally, KX anesthesia is a convenient model to investigate further the mechanisms underlying wake-related ketamine-dependent HFO.<\/jats:p>","DOI":"10.1038\/s41598-021-85705-5","type":"journal-article","created":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T12:47:41Z","timestamp":1616071661000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Network and synaptic mechanisms underlying high frequency oscillations in the rat and cat olfactory bulb under ketamine-xylazine anesthesia"],"prefix":"10.1038","volume":"11","author":[{"given":"W\u0142adys\u0142aw","family":"\u015aredniawa","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacek","family":"Wr\u00f3bel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ewa","family":"Kublik","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel Krzysztof","family":"W\u00f3jcik","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Miles Adrian","family":"Whittington","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark Jeremy","family":"Hunt","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,3,18]]},"reference":[{"key":"85705_CR1","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/S1364-6613(00)01568-0","volume":"5","author":"AK Engel","year":"2001","unstructured":"Engel, A. K. & Singer, W. Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. 5, 16\u201325. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-0 (2001).","journal-title":"Trends Cogn. Sci."},{"key":"85705_CR2","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1152\/physiol.00021.2010","volume":"25","author":"LL Colgin","year":"2010","unstructured":"Colgin, L. L. & Moser, E. I. Gamma oscillations in the hippocampus. Physiology 25, 319\u2013329. https:\/\/doi.org\/10.1152\/physiol.00021.2010 (2010).","journal-title":"Physiology"},{"key":"85705_CR3","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1038\/nrn3241","volume":"13","author":"G Buzs\u00e1ki","year":"2012","unstructured":"Buzs\u00e1ki, G., Anastassiou, C. A. & Koch, C. The origin of extracellular fields and currents\u2014EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 13, 407\u2013420. https:\/\/doi.org\/10.1038\/nrn3241 (2012).","journal-title":"Nat. Rev. Neurosci."},{"key":"85705_CR4","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1126\/science.aan6203","volume":"358","author":"D Khodagholy","year":"2017","unstructured":"Khodagholy, D., Gelinas, J. N. & Buzs\u00e1ki, G. Learning-enhanced coupling between ripple oscillations in association cortices and hippocampus. Science 358, 369\u2013372. https:\/\/doi.org\/10.1126\/science.aan6203 (2017).","journal-title":"Science"},{"key":"85705_CR5","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1152\/jn.00107.2014","volume":"112","author":"D Haufler","year":"2014","unstructured":"Haufler, D. & Pare, D. High-frequency oscillations are prominent in the extended amygdala. J. Neurophysiol. 112, 110\u2013119. https:\/\/doi.org\/10.1152\/jn.00107.2014 (2014).","journal-title":"J. Neurophysiol."},{"key":"85705_CR6","doi-asserted-by":"publisher","first-page":"4519","DOI":"10.1073\/pnas.1617249114","volume":"114","author":"W Zhong","year":"2017","unstructured":"Zhong, W. et al. Selective entrainment of gamma subbands by different slow network oscillations. Proc. Natl. Acad. Sci. U.S.A. 114, 4519\u20134524. https:\/\/doi.org\/10.1073\/pnas.1617249114 (2017).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"85705_CR7","doi-asserted-by":"publisher","first-page":"1131","DOI":"10.1126\/science.aba0672","volume":"367","author":"AP Vaz","year":"2020","unstructured":"Vaz, A. P., Wittig, J. H., Inati, S. K. & Zaghloul, K. A. Replay of cortical spiking sequences during human memory retrieval. Science 367, 1131\u20131134. https:\/\/doi.org\/10.1126\/science.aba0672 (2020).","journal-title":"Science"},{"key":"85705_CR8","doi-asserted-by":"publisher","first-page":"14432","DOI":"10.1073\/pnas.1308285110","volume":"110","author":"J Borjigin","year":"2013","unstructured":"Borjigin, J. et al. Surge of neurophysiological coherence and connectivity in the dying brain. Proc. Natl. Acad. Sci. U.S.A. 110, 14432\u201314437. https:\/\/doi.org\/10.1073\/pnas.1308285110 (2013).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"85705_CR9","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1002\/ana.22548","volume":"71","author":"M Zijlmans","year":"2012","unstructured":"Zijlmans, M. et al. High-frequency oscillations as a new biomarker in epilepsy. Ann. Neurol. 71, 169\u2013178. https:\/\/doi.org\/10.1002\/ana.22548 (2012).","journal-title":"Ann. Neurol."},{"key":"85705_CR10","doi-asserted-by":"publisher","first-page":"2153","DOI":"10.1093\/brain\/awg229","volume":"126","author":"G Foffani","year":"2003","unstructured":"Foffani, G. et al. 300-Hz subthalamic oscillations in Parkinson\u2019s disease. Brain 126, 2153\u201363. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-00 (2003).","journal-title":"Brain"},{"key":"85705_CR11","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1016\/j.biopsych.2006.01.020","volume":"60","author":"MJ Hunt","year":"2006","unstructured":"Hunt, M. J., Raynaud, B. & Garcia, R. Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats. Biol. Psychiat. 60, 1206\u20131214. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-01 (2006).","journal-title":"Biol. Psychiat."},{"key":"85705_CR12","doi-asserted-by":"publisher","first-page":"1170","DOI":"10.1126\/science.290.5494.1170","volume":"290","author":"E Shimizu","year":"2000","unstructured":"Shimizu, E., Tang, Y. P., Rampon, C. & Tsien, J. Z. NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290, 1170\u20131174. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-02 (2000).","journal-title":"Science"},{"key":"85705_CR13","doi-asserted-by":"publisher","first-page":"808","DOI":"10.1177\/0269881110362126","volume":"25","author":"MJ Hunt","year":"2011","unstructured":"Hunt, M. J., Falinska, M., \u0141eski, S., W\u00f3jcik, D. K. & Kasicki, S. Differential effects produced by ketamine on oscillatory activity recorded in the rat hippocampus, dorsal striatum and nucleus accumbens. J. Psychopharmacol. (Oxf., Engl.) 25, 808\u201321. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-03 (2011).","journal-title":"J. Psychopharmacol. (Oxf., Engl.)"},{"key":"85705_CR14","doi-asserted-by":"publisher","first-page":"e21814","DOI":"10.1371\/journal.pone.0021814","volume":"6","author":"MJ Nicol\u00e1s","year":"2011","unstructured":"Nicol\u00e1s, M. J. et al. Ketamine-induced oscillations in the motor circuit of the rat basal ganglia. PLoS One 6, e21814. https:\/\/doi.org\/10.1016\/S1364-6613(00)01568-04 (2011).","journal-title":"PLoS One"},{"key":"85705_CR15","doi-asserted-by":"publisher","DOI":"10.1038\/srep02348","author":"FV Caixeta","year":"2013","unstructured":"Caixeta, F. V., Corn\u00e9lio, A. M., Scheffer-Teixeira, R., Ribeiro, S. & Tort, A. B. Ketamine alters oscillatory coupling in the hippocampus. Sci. Rep. https:\/\/doi.org\/10.1038\/srep02348 (2013).","journal-title":"Sci. Rep."},{"key":"85705_CR16","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1016\/j.neuropharm.2014.05.037","volume":"85","author":"T Hiyoshi","year":"2014","unstructured":"Hiyoshi, T., Kambe, D., Karasawa, J. I. & Chaki, S. Differential effects of NMDA receptor antagonists at lower and higher doses on basal gamma band oscillation power in rat cortical electroencephalograms. Neuropharmacology 85, 384\u2013396. https:\/\/doi.org\/10.1016\/j.neuropharm.2014.05.037 (2014).","journal-title":"Neuropharmacology"},{"key":"85705_CR17","doi-asserted-by":"publisher","first-page":"1375","DOI":"10.1016\/j.euroneuro.2015.04.004","volume":"25","author":"I Cordon","year":"2015","unstructured":"Cordon, I. et al. Coupling in the cortico-basal ganglia circuit is aberrant in the ketamine model of schizophrenia. Eur. Neuropsychopharmacol. 25, 1375\u20131387. https:\/\/doi.org\/10.1016\/j.euroneuro.2015.04.004 (2015).","journal-title":"Eur. Neuropsychopharmacol."},{"key":"85705_CR18","doi-asserted-by":"publisher","DOI":"10.1088\/1741-2560\/12\/5\/056006","author":"F Flores","year":"2015","unstructured":"Flores, F. et al. A PK-PD model of ketamine-induced high-frequency oscillations. J. Neural Eng. https:\/\/doi.org\/10.1088\/1741-2560\/12\/5\/056006 (2015).","journal-title":"J. Neural Eng."},{"key":"85705_CR19","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1016\/j.neuropharm.2017.01.006","volume":"116","author":"J Kealy","year":"2017","unstructured":"Kealy, J., Commins, S. & Lowry, J. P. The effect of NMDA-R antagonism on simultaneously acquired local field potentials and tissue oxygen levels in the brains of freely-moving rats. Neuropharmacology 116, 343\u2013350. https:\/\/doi.org\/10.1016\/j.neuropharm.2017.01.006 (2017).","journal-title":"Neuropharmacology"},{"key":"85705_CR20","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1016\/j.neuroscience.2017.06.039","volume":"358","author":"J Lee","year":"2017","unstructured":"Lee, J., Hudson, M. R., O\u2019Brien, T. J., Nithianantharajah, J. & Jones, N. C. Local NMDA receptor hypofunction evokes generalized effects on gamma and high-frequency oscillations and behavior. Neuroscience 358, 124\u2013136. https:\/\/doi.org\/10.1016\/j.neuroscience.2017.06.039 (2017).","journal-title":"Neuroscience"},{"key":"85705_CR21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-018-29331-8","volume":"8","author":"B Pittman-Polletta","year":"2018","unstructured":"Pittman-Polletta, B., Hu, K. & Kocsis, B. Subunit-specific NMDAR antagonism dissociates schizophrenia subtype-relevant oscillopathies associated with frontal hypofunction and hippocampal hyperfunction. Sci. Rep. 8, 1\u201314. https:\/\/doi.org\/10.1038\/s41598-018-29331-8 (2018).","journal-title":"Sci. Rep."},{"key":"85705_CR22","doi-asserted-by":"publisher","first-page":"61","DOI":"10.3389\/fncir.2018.00061","volume":"12","author":"T Ye","year":"2018","unstructured":"Ye, T. et al. Ten-hour exposure to low-dose ketamine enhances corticostriatal cross-frequency coupling and hippocampal broad-band gamma oscillations. Front. Neural Circ. 12, 61. https:\/\/doi.org\/10.3389\/fncir.2018.00061 (2018).","journal-title":"Front. Neural Circ."},{"key":"85705_CR23","doi-asserted-by":"publisher","first-page":"1948","DOI":"10.1111\/ejn.14373","volume":"50","author":"IH Hansen","year":"2019","unstructured":"Hansen, I. H. et al. Pharmaco-electroencephalographic responses in the rat differ between active and inactive locomotor states. Eur. J. Neurosci. 50, 1948\u20131971. https:\/\/doi.org\/10.1111\/ejn.14373 (2019).","journal-title":"Eur. J. Neurosci."},{"key":"85705_CR24","doi-asserted-by":"publisher","first-page":"107745","DOI":"10.1016\/j.neuropharm.2019.107745","volume":"158","author":"M Amat-Foraster","year":"2019","unstructured":"Amat-Foraster, M. et al. Modulation of thalamo-cortical activity by the NMDA receptor antagonists ketamine and phencyclidine in the awake freely-moving rat. Neuropharmacology 158, 107745. https:\/\/doi.org\/10.1016\/j.neuropharm.2019.107745 (2019).","journal-title":"Neuropharmacology"},{"key":"85705_CR25","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-020-75641-1","author":"J Wr\u00f3bel","year":"2020","unstructured":"Wr\u00f3bel, J. et al. Nasal respiration is necessary for ketamine-dependent high frequency network oscillations and behavioral hyperactivity in rats. Sci. Rep. https:\/\/doi.org\/10.1038\/s41598-020-75641-1 (2020).","journal-title":"Sci. Rep."},{"key":"85705_CR26","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1038\/s41386-018-0173-y","volume":"44","author":"MJ Hunt","year":"2019","unstructured":"Hunt, M. J. et al. The olfactory bulb is a source of high-frequency oscillations 130\u2013180 Hz associated with a subanesthetic dose of ketamine in rodents. Neuropsychopharmacology 44, 435\u2013442. https:\/\/doi.org\/10.1038\/s41386-018-0173-y (2019).","journal-title":"Neuropsychopharmacology"},{"key":"85705_CR27","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms4572","author":"J Ito","year":"2014","unstructured":"Ito, J. et al. Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration. Nat. Commun.https:\/\/doi.org\/10.1038\/ncomms4572 (2014).","journal-title":"Nat. Commun."},{"key":"85705_CR28","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1093\/bja\/aev095","volume":"114","author":"D Pal","year":"2015","unstructured":"Pal, D., Hambrecht-Wiedbusch, V. S., Silverstein, B. H. & Mashour, G. A. Electroencephalographic coherence and cortical acetylcholine during ketamine-induced unconsciousness. Br. J. Anaesth. 114, 979\u2013989. https:\/\/doi.org\/10.1093\/bja\/aev095 (2015).","journal-title":"Br. J. Anaesth."},{"key":"85705_CR29","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.neuroscience.2009.08.047","volume":"164","author":"MJ Hunt","year":"2009","unstructured":"Hunt, M. J., Matulewicz, P., Gottesmann, C. & Kasicki, S. State-dependent changes in high-frequency oscillations recorded in the rat nucleus accumbens. Neuroscience 164, 380\u2013386. https:\/\/doi.org\/10.1016\/j.neuroscience.2009.08.047 (2009).","journal-title":"Neuroscience"},{"key":"85705_CR30","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0006755","author":"T Hakami","year":"2009","unstructured":"Hakami, T. et al. NMDA receptor hypofunction leads to generalized and persistent aberrant $$\\gamma$$ oscillations independent of hyperlocomotion and the state of consciousness. PLoS ONEhttps:\/\/doi.org\/10.1371\/journal.pone.0006755 (2009).","journal-title":"PLoS ONE"},{"key":"85705_CR31","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.2005458","author":"S Bagur","year":"2018","unstructured":"Bagur, S. et al. Harnessing olfactory bulb oscillations to perform fully brain-based sleep-scoring and real-time monitoring of anaesthesia depth. PLoS Biol.https:\/\/doi.org\/10.1371\/journal.pbio.2005458 (2018).","journal-title":"PLoS Biol."},{"key":"85705_CR32","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1523\/jneurosci.15-01-00030.1995","volume":"15","author":"A Ylinen","year":"1995","unstructured":"Ylinen, A. et al. Sharp wave-associated high-frequency oscillation (200 hz) in the intact hippocampus: Network and intracellular mechanisms. J. Neurosci. 15, 30\u201346. https:\/\/doi.org\/10.1523\/jneurosci.15-01-00030.1995 (1995).","journal-title":"J. Neurosci."},{"key":"85705_CR33","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.1152\/jn.2001.86.4.1884","volume":"86","author":"F Grenier","year":"2001","unstructured":"Grenier, F., Timofeev, I. & Steriade, M. Focal synchronization of ripples (80\u2013200 Hz) in neocortex and their neuronal correlates. J. Neurophysiol. 86, 1884\u20131898. https:\/\/doi.org\/10.1152\/jn.2001.86.4.1884 (2001).","journal-title":"J. Neurophysiol."},{"key":"85705_CR34","doi-asserted-by":"publisher","first-page":"908","DOI":"10.1152\/jn.00261.2013","volume":"111","author":"R Chery","year":"2014","unstructured":"Chery, R., Gurden, H. & Martin, C. Anesthetic regimes modulate the temporal dynamics of local field potential in the mouse olfactory bulb. J. Neurophysiol. 111, 908\u2013917. https:\/\/doi.org\/10.1152\/jn.00261.2013 (2014).","journal-title":"J. Neurophysiol."},{"key":"85705_CR35","doi-asserted-by":"publisher","first-page":"1010","DOI":"10.1016\/j.neuron.2013.07.025","volume":"80","author":"G Lepousez","year":"2013","unstructured":"Lepousez, G. & Lledo, P. M. Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 80, 1010\u20131024. https:\/\/doi.org\/10.1016\/j.neuron.2013.07.025 (2013).","journal-title":"Neuron"},{"key":"85705_CR36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-020-66023-8","volume":"10","author":"AU Nicol","year":"2020","unstructured":"Nicol, A. U. & Morton, A. J. Characteristic patterns of EEG oscillations in sheep (Ovis aries) induced by ketamine may explain the psychotropic effects seen in humans. Sci. Rep. 10, 1\u201310. https:\/\/doi.org\/10.1038\/s41598-020-66023-8 (2020).","journal-title":"Sci. Rep."},{"key":"85705_CR37","doi-asserted-by":"publisher","DOI":"10.1007\/s12021-020-09487-3","author":"GJ Jurkiewicz","year":"2020","unstructured":"Jurkiewicz, G. J., Hunt, M. J. & \u017bygierewicz, J. Addressing pitfalls in phase-amplitude coupling analysis with an extended modulation index toolbox. Neuroinformaticshttps:\/\/doi.org\/10.1007\/s12021-020-09487-3 (2020).","journal-title":"Neuroinformatics"},{"key":"85705_CR38","doi-asserted-by":"publisher","first-page":"1032","DOI":"10.1016\/j.celrep.2015.01.047","volume":"10","author":"AM Boyd","year":"2015","unstructured":"Boyd, A. M., Kato, H. K., Komiyama, T. & Isaacson, J. S. Broadcasting of cortical activity to the olfactory bulb. Cell Rep. 10, 1032\u20131039. https:\/\/doi.org\/10.1016\/j.celrep.2015.01.047 (2015).","journal-title":"Cell Rep."},{"key":"85705_CR39","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms12238","volume":"7","author":"A Diodato","year":"2016","unstructured":"Diodato, A. et al. Molecular signatures of neural connectivity in the olfactory cortex. Nat. Commun. 7, 1\u201310. https:\/\/doi.org\/10.1038\/ncomms12238 (2016).","journal-title":"Nat. Commun."},{"key":"85705_CR40","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.1016\/j.neuron.2012.10.020","volume":"76","author":"AM Boyd","year":"2012","unstructured":"Boyd, A. M., Sturgill, J. F., Poo, C. & Isaacson, J. S. Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161\u20131174. https:\/\/doi.org\/10.1016\/j.neuron.2012.10.020 (2012).","journal-title":"Neuron"},{"key":"85705_CR41","doi-asserted-by":"publisher","first-page":"3921","DOI":"10.1152\/jn.00475.2003","volume":"90","author":"KR Neville","year":"2003","unstructured":"Neville, K. R. & Haberly, L. B. Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J. Neurophysiol. 90, 3921\u20133930. https:\/\/doi.org\/10.1152\/jn.00475.2003 (2003).","journal-title":"J. Neurophysiol."},{"key":"85705_CR42","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1113\/jphysiol.1942.sp003955","volume":"100","author":"ED Adrian","year":"1942","unstructured":"Adrian, E. D. Olfactory reactions in the brain of the hedgehog. J. Physiol. 100, 459\u2013473. https:\/\/doi.org\/10.1113\/jphysiol.1942.sp003955 (1942).","journal-title":"J. Physiol."},{"key":"85705_CR43","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1126\/science.175.4017.84","volume":"175","author":"F Macrides","year":"1972","unstructured":"Macrides, F. & Chorover, S. L. Olfactory bulb units: Activity correlated with inhalation cycles and odor quality. Science 175, 84\u201387. https:\/\/doi.org\/10.1126\/science.175.4017.84 (1972).","journal-title":"Science"},{"key":"85705_CR44","doi-asserted-by":"publisher","first-page":"30","DOI":"10.3389\/fnana.2012.00030","volume":"6","author":"H Hintiryan","year":"2012","unstructured":"Hintiryan, H. et al. Comprehensive connectivity of the mouse main olfactory bulb: Analysis and online digital atlas. Front. Neuroanat. 6, 30. https:\/\/doi.org\/10.3389\/fnana.2012.00030 (2012).","journal-title":"Front. Neuroanat."},{"key":"85705_CR45","doi-asserted-by":"publisher","first-page":"320","DOI":"10.1016\/j.neuron.2012.05.017","volume":"75","author":"I Fukunaga","year":"2012","unstructured":"Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A. T. Two distinct channels of olfactory bulb output. Neuron 75, 320\u2013329. https:\/\/doi.org\/10.1016\/j.neuron.2012.05.017 (2012).","journal-title":"Neuron"},{"key":"85705_CR46","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1152\/jn.1975.38.2.356","volume":"38","author":"C Nicholson","year":"1975","unstructured":"Nicholson, C. & Freeman, J. A. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J. Neurophysiol. 38, 356\u2013368. https:\/\/doi.org\/10.1007\/s12021-020-09487-30 (1975).","journal-title":"J. Neurophysiol."},{"key":"85705_CR47","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1152\/physrev.1985.65.1.37","volume":"65","author":"U Mitzdorf","year":"1985","unstructured":"Mitzdorf, U. Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37\u2013100 (1985).","journal-title":"Physiol. Rev."},{"key":"85705_CR48","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1016\/B978-0-444-63350-7.00009-7","volume":"208","author":"LM Kay","year":"2014","unstructured":"Kay, L. M. Circuit oscillations in odor perception and memory. Progr. Brain Res. 208, 223\u2013251. https:\/\/doi.org\/10.1016\/B978-0-444-63350-7.00009-7 (2014).","journal-title":"Progr. Brain Res."},{"key":"85705_CR49","doi-asserted-by":"publisher","first-page":"88","DOI":"10.3389\/fncir.2014.00088","volume":"8","author":"N Fourcaud-Trocm\u00e9","year":"2014","unstructured":"Fourcaud-Trocm\u00e9, N., Courtiol, E. & Buonviso, N. Two distinct olfactory bulb sublaminar networks involved in gamma and beta oscillation generation: A CSD study in the anesthetized rat. Front. Neural Circ. 8, 88. https:\/\/doi.org\/10.3389\/fncir.2014.00088 (2014).","journal-title":"Front. Neural Circ."},{"key":"85705_CR50","doi-asserted-by":"publisher","first-page":"2097","DOI":"10.1113\/jphysiol.2013.269886","volume":"592","author":"SD Burton","year":"2014","unstructured":"Burton, S. D. & Urban, N. N. Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells. J. Physiol. 592, 2097\u20132118. https:\/\/doi.org\/10.1113\/jphysiol.2013.269886 (2014).","journal-title":"J. Physiol."},{"key":"85705_CR51","doi-asserted-by":"publisher","first-page":"14777","DOI":"10.1073\/pnas.1310686110","volume":"110","author":"A Nunez-Parra","year":"2013","unstructured":"Nunez-Parra, A., Maurer, R. K., Krahe, K., Smith, R. S. & Araneda, R. C. Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proc. Natl. Acad. Sci. U.S.A. 110, 14777\u201382. https:\/\/doi.org\/10.1073\/pnas.1310686110 (2013).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"85705_CR52","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1016\/S0896-6273(00)81065-X","volume":"25","author":"WR Chen","year":"2000","unstructured":"Chen, W. R., Xiong, W. & Shepherd, G. M. Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 25, 625\u2013633. https:\/\/doi.org\/10.1016\/S0896-6273(00)81065-X (2000).","journal-title":"Neuron"},{"key":"85705_CR53","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1515\/REVNEURO.2002.13.1.1","volume":"13","author":"RD Traub","year":"2002","unstructured":"Traub, R. D. et al. Axonal gap junctions between principal neurons: A novel source of network oscillations, and perhaps epileptogenesis. Rev. Neurosci. 13, 1\u201330. https:\/\/doi.org\/10.1515\/REVNEURO.2002.13.1.1 (2002).","journal-title":"Rev. Neurosci."},{"key":"85705_CR54","doi-asserted-by":"publisher","first-page":"2269","DOI":"10.1523\/JNEUROSCI.4791-05.2006","volume":"26","author":"JM Christie","year":"2006","unstructured":"Christie, J. M. & Westbrook, G. L. Lateral excitation within the olfactory bulb. J. Neurosci. 26, 2269\u20132277. https:\/\/doi.org\/10.1523\/JNEUROSCI.4791-05.2006 (2006).","journal-title":"J. Neurosci."},{"key":"85705_CR55","doi-asserted-by":"publisher","first-page":"1359","DOI":"10.1016\/j.neuropharm.2011.04.006","volume":"62","author":"KG Phillips","year":"2012","unstructured":"Phillips, K. G. et al. Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 62, 1359\u20131370. https:\/\/doi.org\/10.1016\/j.neuropharm.2011.04.006 (2012).","journal-title":"Neuropharmacology"},{"key":"85705_CR56","doi-asserted-by":"publisher","first-page":"1090","DOI":"10.1152\/jn.00090.2018","volume":"120","author":"BL Osinski","year":"2018","unstructured":"Osinski, B. L., Kim, A., Xiao, W., Mehta, N. M. & Kay, L. M. Pharmacological manipulation of the olfactory bulb modulates beta oscillations: Testing model predictions. J. Neurophysiol. 120, 1090\u20131106. https:\/\/doi.org\/10.1152\/jn.00090.2018 (2018).","journal-title":"J. Neurophysiol."},{"key":"85705_CR57","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/0006-8993(96)00083-2","volume":"719","author":"DA Wilson","year":"1996","unstructured":"Wilson, D. A., Sullivan, R. M., Gall, C. M. & Guthrie, K. M. NMDA-receptor modulation of lateral inhibition and c-fos expression in olfactory bulb. Brain Res. 719, 62\u201371. https:\/\/doi.org\/10.1016\/B978-0-444-63350-7.00009-70 (1996).","journal-title":"Brain Res."},{"key":"85705_CR58","doi-asserted-by":"publisher","first-page":"2034","DOI":"10.1152\/jn.00109.2017","volume":"118","author":"SD Burton","year":"2017","unstructured":"Burton, S. D. Inhibitory circuits of the mammalian main olfactory bulb. J. Neurophysiol. 118, 2034\u20132051. https:\/\/doi.org\/10.1016\/B978-0-444-63350-7.00009-71 (2017).","journal-title":"J. Neurophysiol."},{"key":"85705_CR59","doi-asserted-by":"publisher","first-page":"1401","DOI":"10.1002\/ar.22732","volume":"296","author":"C Crespo","year":"2013","unstructured":"Crespo, C., Liberia, T., Blasco-Ib\u00e1\u00f1ez, J. M., N\u00e1cher, J. & Varea, E. The circuits of the olfactory bulb: The exception as a rule. Anat. Rec. 296, 1401\u20131412. https:\/\/doi.org\/10.1016\/B978-0-444-63350-7.00009-72 (2013).","journal-title":"Anat. Rec."},{"key":"85705_CR60","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1007\/BF00239586","volume":"99","author":"K Kosaka","year":"1994","unstructured":"Kosaka, K., Heizmann, C. W. & Kosaka, T. Calcium-binding protein parvalbumin-immunoreactive neurons in the rat olfactory bulb\u20131. Distribution and structural features in adult rat. Exp. Brain Res. 99, 191\u2013204. https:\/\/doi.org\/10.1007\/BF00239586 (1994).","journal-title":"Exp. Brain Res."},{"key":"85705_CR61","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1126\/science.aal3231","volume":"75","author":"G Mountoufaris","year":"2017","unstructured":"Mountoufaris, G. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 75, 793\u2013807. https:\/\/doi.org\/10.1126\/science.aal3231 (2017).","journal-title":"Nat. Rev. Neurosci."},{"key":"85705_CR62","doi-asserted-by":"publisher","first-page":"1218","DOI":"10.1016\/j.neuron.2013.08.036","volume":"80","author":"HK Kato","year":"2013","unstructured":"Kato, H. K., Gillet, S. N., Peters, A. J., Isaacson, J. S. & Komiyama, T. Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80, 1218\u20131231. https:\/\/doi.org\/10.1016\/j.neuron.2013.08.036 (2013).","journal-title":"Neuron"},{"key":"85705_CR63","doi-asserted-by":"publisher","first-page":"1232","DOI":"10.1016\/j.neuron.2013.08.027","volume":"80","author":"K Miyamichi","year":"2013","unstructured":"Miyamichi, K. et al. Dissecting local circuits: Parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232\u201345. https:\/\/doi.org\/10.1016\/j.neuron.2013.08.027 (2013).","journal-title":"Neuron"},{"key":"85705_CR64","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1017\/S1461145712001034","volume":"16","author":"M Olszewski","year":"2013","unstructured":"Olszewski, M., Piasecka, J., Goda, S. A., Kasicki, S. & Hunt, M. J. Antipsychotic compounds differentially modulate high-frequency oscillations in the rat nucleus accumbens: A comparison of first- and second-generation drugs. Int. J. Neuropsychopharmacol. 16, 1009\u20131020. https:\/\/doi.org\/10.1017\/S1461145712001034 (2013).","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"85705_CR65","doi-asserted-by":"publisher","first-page":"972","DOI":"10.1177\/0269881113495117","volume":"27","author":"MJ Hunt","year":"2013","unstructured":"Hunt, M. J. & Kasicki, S. A systematic review of the effects of NMDA receptor antagonists on oscillatory activity recorded in vivo. J. Psychopharmacol. 27, 972\u2013986. https:\/\/doi.org\/10.1177\/0269881113495117 (2013).","journal-title":"J. Psychopharmacol."},{"key":"85705_CR66","unstructured":"Hansen, I.\u00a0H. Investigation of Pharmacological Manipulationon Brain Connectivity in Rats and Humans for Improvement of Drug Development. Ph.D. thesis, DTU Health Technology (2019)."},{"key":"85705_CR67","first-page":"344","volume":"50","author":"MB Struck","year":"2011","unstructured":"Struck, M. B., Andrutis, K. A., Ramirez, H. E. & Battles, A. H. Effect of a short-term fast on ketamine-xylazine anesthesia in rats. J. Am. Assoc. Lab. Anim. Sci. JAALAS 50, 344 (2011).","journal-title":"J. Am. Assoc. Lab. Anim. Sci. JAALAS"},{"key":"85705_CR68","doi-asserted-by":"publisher","first-page":"e1005893","DOI":"10.1371\/journal.pcbi.1005893","volume":"13","author":"T Dupr\u00e9 la Tour","year":"2017","unstructured":"Dupr\u00e9 la Tour, T. et al. Non-linear auto-regressive models for cross-frequency coupling in neural time series. PLoS Comput. Biol. 13, e1005893. https:\/\/doi.org\/10.1371\/journal.pcbi.1005893 (2017).","journal-title":"PLoS Comput. Biol."},{"key":"85705_CR69","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1162\/NECO_a_00236","volume":"24","author":"J Potworowski","year":"2012","unstructured":"Potworowski, J., Jakuczun, W., \u0141eski, S. & W\u00f3jcik, D. Kernel current source density method. Neural Comput. 24, 541\u2013575. https:\/\/doi.org\/10.1162\/NECO_a_00236 (2012).","journal-title":"Neural Comput."},{"key":"85705_CR70","first-page":"2","volume":"708511","author":"HC Chintaluri","year":"2019","unstructured":"Chintaluri, H. C. et al. kCSD-python, a tool for reliable current source density estimation. BioRxiv 708511, 2 (2019).","journal-title":"BioRxiv"},{"key":"85705_CR71","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1109\/MCSE.2007.55","volume":"9","author":"JD Hunter","year":"2007","unstructured":"Hunter, J. D. Matplotlib: A 2D graphics environment. Comput. Sci. Eng. 9, 90\u201395. https:\/\/doi.org\/10.1109\/MCSE.2007.55 (2007).","journal-title":"Comput. Sci. Eng."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85705-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85705-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85705-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T00:42:28Z","timestamp":1670028148000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-85705-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,18]]},"references-count":71,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["85705"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-85705-5","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.07.23.217604","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,18]]},"assertion":[{"value":"23 July 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 February 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 March 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"6390"}}