{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,12]],"date-time":"2026-03-12T02:56:06Z","timestamp":1773284166669,"version":"3.50.1"},"reference-count":69,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,8,2]],"date-time":"2018-08-02T00:00:00Z","timestamp":1533168000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2018,8,2]],"date-time":"2018-08-02T00:00:00Z","timestamp":1533168000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["DMS-1042134"],"award-info":[{"award-number":["DMS-1042134"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100006955","name":"Office of Extramural Research, National Institutes of Health","doi-asserted-by":"publisher","award":["HL102241"],"award-info":[{"award-number":["HL102241"]}],"id":[{"id":"10.13039\/100006955","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100006955","name":"Office of Extramural Research, National Institutes of Health","doi-asserted-by":"publisher","award":["AG048108"],"award-info":[{"award-number":["AG048108"]}],"id":[{"id":"10.13039\/100006955","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100006955","name":"Office of Extramural Research, National Institutes of Health","doi-asserted-by":"publisher","award":["MH100820"],"award-info":[{"award-number":["MH100820"]}],"id":[{"id":"10.13039\/100006955","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100006955","name":"Office of Extramural Research, National Institutes of Health","doi-asserted-by":"publisher","award":["ES006189"],"award-info":[{"award-number":["ES006189"]}],"id":[{"id":"10.13039\/100006955","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>NMDAR antagonism alters mesolimbic, hippocampal, and cortical function, acutely reproducing the positive, cognitive, and negative symptoms of schizophrenia. These physiological and behavioral effects may depend differentially on NMDAR subtype- and region-specific effects. The dramatic electrophysiological signatures of NMDAR blockade in rodents include potentiated high frequency oscillations (HFOs, \u223c140\u2009Hz), likely generated in mesolimbic structures, and increased HFO phase-amplitude coupling (PAC), a phenomenon related to goal-directed behavior and dopaminergic tone. This study examined the impact of subtype-specific NMDAR antagonism on HFOs and PAC. We found that positive-symptom-associated NR2A-preferring antagonism (NVP-AAM077), but not NR2B-specific antagonism (Ro25-6985) or saline control, replicated increases in HFO power seen with nonspecific antagonism (MK-801). However, PAC following NR2A-preferring antagonism was distinct from all other conditions. While \u03b8-HFO PAC was prominent or potentiated in other conditions, NVP-AAM077 increased \u03b4-HFO PAC and decreased \u03b8-HFO PAC. Furthermore, active wake epochs exhibiting narrowband frontal \u03b4 oscillations, and not broadband sleep-associated \u03b4, selectively exhibited \u03b4-HFO coupling, while paradoxical sleep epochs having a high CA1 \u03b8 to frontal \u03b4 ratio selectively exhibited \u03b8-HFO coupling. Our results suggest: (1) NR2A-preferring antagonism induces oscillopathies reflecting frontal hyperfunction and hippocampal hypofunction; and (2) HFO PAC indexes cortical vs. hippocampal control of mesolimbic circuits.<\/jats:p>","DOI":"10.1038\/s41598-018-29331-8","type":"journal-article","created":{"date-parts":[[2018,7,27]],"date-time":"2018-07-27T04:56:01Z","timestamp":1532667361000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":28,"title":["Subunit-specific NMDAR antagonism dissociates schizophrenia subtype-relevant oscillopathies associated with frontal hypofunction and hippocampal hyperfunction"],"prefix":"10.1038","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6798-7191","authenticated-orcid":false,"given":"Benjamin","family":"Pittman-Polletta","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kun","family":"Hu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bernat","family":"Kocsis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2018,8,2]]},"reference":[{"key":"29331_CR1","doi-asserted-by":"publisher","first-page":"523","DOI":"10.1016\/S0022-3956(99)00029-1","volume":"33","author":"JW Olney","year":"1999","unstructured":"Olney, J. W., Newcomer, J. W. & Farber, N. B. NMDA receptor hypofunction model of schizophrenia. Journal of Psychiatric Research 33, 523\u2013533 (1999).","journal-title":"Journal of Psychiatric Research"},{"key":"29331_CR2","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1093\/schbul\/sbr133","volume":"38","author":"A Adell","year":"2011","unstructured":"Adell, A., Jim\u00e9nez-S\u00e1nchez, L., L\u00f3pez-Gil, X. & Rom\u00f3n, T. Is the acute nmda receptor hypofunction a valid model of schizophrenia? Schizophr. Bull. 38, 9\u201314 (2011).","journal-title":"Schizophr. Bull."},{"key":"29331_CR3","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1176\/appi.ajp.2014.14040435","volume":"172","author":"J Arnedo","year":"2015","unstructured":"Arnedo, J. et al. Uncovering the hidden risk architecture of the schizophrenias: confirmation in three independent genome-wide association studies. Am. J. Psychiatry 172, 139\u2013153 (2015).","journal-title":"Am. J. Psychiatry"},{"key":"29331_CR4","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. Psychiatry 60, 1206\u20131214 (2006).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR5","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 (2011).","journal-title":"PLoS ONE"},{"key":"29331_CR6","doi-asserted-by":"crossref","unstructured":"Caixeta, F. V., Corn\u00e9lio, A. M., Scheffer-Teixeira, R., Ribeiro, S. & Tort, A. B. Ketamine alters oscillatory coupling in the hippocampus. Sci. Reports 3 (2013).","DOI":"10.1038\/srep02348"},{"key":"29331_CR7","doi-asserted-by":"crossref","unstructured":"Cordon, I. et al. Coupling in the cortico-basal ganglia circuit is aberrant in the ketamine model of schizophrenia. Eur. Neuropsychopharmacol. (2015).","DOI":"10.1016\/j.euroneuro.2015.04.004"},{"key":"29331_CR8","doi-asserted-by":"publisher","first-page":"600","DOI":"10.1523\/JNEUROSCI.3481-08.2009","volume":"29","author":"X Chen","year":"2009","unstructured":"Chen, X., Shu, S. & Bayliss, D. A. Hcn1 channel subunits are a molecular substrate for hypnotic actions of ketamine. J. Neurosci. 29, 600\u2013609 (2009).","journal-title":"J. Neurosci."},{"key":"29331_CR9","doi-asserted-by":"publisher","first-page":"931","DOI":"10.1177\/0269881109102539","volume":"24","author":"M Hunt","year":"2010","unstructured":"Hunt, M., Falinska, M. & Kasicki, S. Local injection of mk801 modifies oscillatory activity in the nucleus accumbens in awake rats. J. Psychopharmacol. 24, 931\u2013941 (2010).","journal-title":"J. Psychopharmacol."},{"key":"29331_CR10","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 (2013).","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"29331_CR11","doi-asserted-by":"publisher","first-page":"1020","DOI":"10.1016\/j.biopsych.2015.02.005","volume":"77","author":"BR Pittman-Polletta","year":"2015","unstructured":"Pittman-Polletta, B. R., Kocsis, B., Vijayan, S., Whittington, M. A. & Kopell, N. J. Brain rhythms connect impaired inhibition to altered cognition in schizophrenia. Biol. Psychiatry 77, 1020\u20131030 (2015).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR12","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1111\/cns.12081","volume":"19","author":"B Kocsis","year":"2013","unstructured":"Kocsis, B., Brown, R. E., McCarley, R. W. & Hajos, M. Impact of ketamine on neuronal network dynamics: translational modeling of schizophrenia-relevant deficits. CNS Neurosci. & Ther. 19, 437\u2013447 (2013).","journal-title":"CNS Neurosci. & Ther."},{"key":"29331_CR13","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 (2013).","journal-title":"J. Psychopharmacol."},{"key":"29331_CR14","doi-asserted-by":"publisher","first-page":"987","DOI":"10.1016\/j.biopsych.2011.10.002","volume":"71","author":"B Kocsis","year":"2012","unstructured":"Kocsis, B. Differential role of NR2A and NR2B subunits in N-methyl-D-aspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol. Psychiatry 71, 987\u2013995 (2012).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR15","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1007\/s11055-016-0337-3","volume":"46","author":"A Serkov","year":"2016","unstructured":"Serkov, A. & Maiorov, V. \u03b4 and \u03b8 modulation of fast \u03b3 activity in the ventral tegmental area of the midbrain in rats during a conditioned avoidance reflex. Neurosci. Behav. Physiol. 46, 957\u2013963 (2016).","journal-title":"Neurosci. Behav. Physiol."},{"key":"29331_CR16","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 (2014).","journal-title":"J. Neurophysiol."},{"key":"29331_CR17","doi-asserted-by":"publisher","first-page":"776","DOI":"10.1007\/s11055-016-0310-1","volume":"46","author":"A Serkov","year":"2016","unstructured":"Serkov, A., Serkova, V. & Maiorov, V. Interaction of the medial prefrontal cortex, ventral hippocampus, and basolateral amygdala during performance of a conditioned avoidance reflex. Neurosci. Behav. Physiol. 46, 776\u2013782 (2016).","journal-title":"Neurosci. Behav. Physiol."},{"key":"29331_CR18","doi-asserted-by":"publisher","first-page":"808","DOI":"10.1177\/0269881110362126","volume":"25","author":"MJ Hunt","year":"2011","unstructured":"Hunt, M. J., Falinska, M., Lkeski, 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. 25, 808\u2013821 (2011).","journal-title":"J. Psychopharmacol."},{"key":"29331_CR19","doi-asserted-by":"publisher","first-page":"1795","DOI":"10.1016\/j.euroneuro.2013.01.012","volume":"23","author":"M Olszewski","year":"2013","unstructured":"Olszewski, M., Dolowa, W., Matulewicz, P., Kasicki, S. & Hunt, M. J. Nmda receptor antagonist-enhanced high frequency oscillations: Are they generated broadly or regionally specific? Eur. Neuropsychopharmacol. 23, 1795\u20131805 (2013).","journal-title":"Eur. Neuropsychopharmacol."},{"key":"29331_CR20","doi-asserted-by":"publisher","first-page":"893","DOI":"10.1016\/S0306-4522(97)00239-X","volume":"81","author":"RP Vertes","year":"1997","unstructured":"Vertes, R. P. & Kocsis, B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocam- pus. Neurosci. 81, 893\u2013926 (1997).","journal-title":"Neurosci."},{"key":"29331_CR21","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1016\/S0896-6273(02)00586-X","volume":"33","author":"G Buzs\u00e1ki","year":"2002","unstructured":"Buzs\u00e1ki, G. Theta oscillations in the hippocampus. Neuron 33, 325\u2013340 (2002).","journal-title":"Neuron"},{"key":"29331_CR22","doi-asserted-by":"publisher","first-page":"10750","DOI":"10.1523\/JNEUROSCI.0735-13.2013","volume":"33","author":"LM Carracedo","year":"2013","unstructured":"Carracedo, L. M. et al. A neocortical delta rhythm facilitates reciprocal interlaminar interactions via nested theta rhythms. The J. Neurosci. 33, 10750\u201310761 (2013).","journal-title":"The J. Neurosci."},{"key":"29331_CR23","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.neuron.2011.08.018","volume":"72","author":"S Fujisawa","year":"2011","unstructured":"Fujisawa, S. & Buzs\u00e1ki, G. A 4 hz oscillation adaptively synchronizes prefrontal, vta, and hippocampal activities. Neuron. 72, 153\u2013165 (2011).","journal-title":"Neuron."},{"key":"29331_CR24","doi-asserted-by":"crossref","unstructured":"Roy, A., Svensson, F. P., Mazeh, A. & Kocsis, B. Prefrontal-hippocampal coupling by theta rhythm and by 2\u20135 hz oscillation in the delta band: The role of the nucleus reuniens of the thalamus. Brain Struct. Funct. 1\u201312 (2017).","DOI":"10.1007\/s00429-017-1374-6"},{"key":"29331_CR25","doi-asserted-by":"publisher","first-page":"3622","DOI":"10.1523\/JNEUROSCI.15-05-03622.1995","volume":"15","author":"P O\u2019Donnell","year":"1995","unstructured":"O\u2019Donnell, P. & Grace, A. A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. The J. Neurosci. 15, 3622\u20133639 (1995).","journal-title":"The J. Neurosci."},{"key":"29331_CR26","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/j.neuron.2005.06.017","volume":"47","author":"Y Goto","year":"2005","unstructured":"Goto, Y. & Grace, A. A. Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron 47, 255\u2013266 (2005).","journal-title":"Neuron"},{"key":"29331_CR27","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1016\/j.tins.2008.08.002","volume":"31","author":"Y Goto","year":"2008","unstructured":"Goto, Y. & Grace, A. A. Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci. 31, 552\u2013558 (2008).","journal-title":"Trends Neurosci."},{"key":"29331_CR28","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1038\/nn1471","volume":"8","author":"Y Goto","year":"2005","unstructured":"Goto, Y. & Grace, A. A. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci. 8, 805 (2005).","journal-title":"Nat. Neurosci."},{"key":"29331_CR29","doi-asserted-by":"publisher","first-page":"e5062","DOI":"10.1371\/journal.pone.0005062","volume":"4","author":"AJ Gruber","year":"2009","unstructured":"Gruber, A. J., Hussain, R. J. & O\u2019Donnell, P. The nucleus accumbens: a switchboard for goal-directed behaviors. PLoS ONE 4, e5062 (2009).","journal-title":"PLoS ONE"},{"key":"29331_CR30","doi-asserted-by":"publisher","first-page":"4915","DOI":"10.1523\/JNEUROSCI.21-13-04915.2001","volume":"21","author":"SB Floresco","year":"2001","unstructured":"Floresco, S. B., Todd, C. L. & Grace, A. A. Glutamatergic afferents from the hippocampus to the nucleus accumbens regulate activity of ventral tegmental area dopamine neurons. J. Neurosci. 21, 4915\u20134922 (2001).","journal-title":"J. Neurosci."},{"key":"29331_CR31","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1038\/nn1103","volume":"6","author":"SB Floresco","year":"2003","unstructured":"Floresco, S. B., West, A. R., Ash, B., Moore, H. & Grace, A. A. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat. Neurosci. 6, 968 (2003).","journal-title":"Nat. Neurosci."},{"key":"29331_CR32","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.1038\/sj.npp.1300963","volume":"31","author":"DJ Lodge","year":"2006","unstructured":"Lodge, D. J. & Grace, A. A. The hippocampus modulates dopamine neuron responsivity by regulating the intensity of phasic neuron activation. Neuropsychopharmacol. 31, 1356 (2006).","journal-title":"Neuropsychopharmacol."},{"key":"29331_CR33","doi-asserted-by":"publisher","first-page":"16865","DOI":"10.1523\/JNEUROSCI.2449-13.2013","volume":"33","author":"MH Patton","year":"2013","unstructured":"Patton, M. H., Bizup, B. T. & Grace, A. A. The infralimbic cortex bidirectionally modulates mesolimbic dopamine neuron activity via distinct neural pathways. J. Neurosci. 33, 16865\u201316873 (2013).","journal-title":"J. Neurosci."},{"key":"29331_CR34","doi-asserted-by":"publisher","first-page":"1011","DOI":"10.5665\/sleep.1972","volume":"35","author":"B Kocsis","year":"2012","unstructured":"Kocsis, B. State-dependent increase of cortical gamma activity during rem sleep after selective blockade of nr2b subunit containing nmda receptors. Sleep 35, 1011\u20131016 (2012).","journal-title":"Sleep"},{"key":"29331_CR35","doi-asserted-by":"publisher","first-page":"1195","DOI":"10.1152\/jn.00106.2010","volume":"104","author":"AB Tort","year":"2010","unstructured":"Tort, A. B., Komorowski, R., Eichenbaum, H. & Kopell, N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J. Neurophysiol. 104, 1195\u20131210 (2010).","journal-title":"J. Neurophysiol."},{"key":"29331_CR36","doi-asserted-by":"publisher","first-page":"730","DOI":"10.1016\/j.biopsych.2007.10.006","volume":"63","author":"D Pinault","year":"2008","unstructured":"Pinault, D. N-methyl d-aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant \u03b3 oscillations in the rat neocortex. Biol. Psychiatry 63, 730\u2013735 (2008).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR37","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1007\/s00429-011-0351-8","volume":"217","author":"K Kittelberger","year":"2012","unstructured":"Kittelberger, K., Hur, E. E., Sazegar, S., Keshavan, V. & Kocsis, B. Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: relevance for the NMDA receptor hypofunction model of schizophrenia. Brain Structure and Function 217, 395\u2013409 (2012).","journal-title":"Brain Structure and Function"},{"key":"29331_CR38","doi-asserted-by":"publisher","first-page":"15085","DOI":"10.1073\/pnas.1314681110","volume":"110","author":"V Na\u00b4cher","year":"2013","unstructured":"Na\u00b4cher, V., Ledberg, A., Deco, G. & Romo, R. Coherent delta-band oscillations between cortical areas correlate with decision making. Proc. Natl. Acad. Sci. 110, 15085\u201315090 (2013).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"29331_CR39","doi-asserted-by":"publisher","first-page":"e28489","DOI":"10.1371\/journal.pone.0028489","volume":"6","author":"C Scheffz\u00fck","year":"2011","unstructured":"Scheffz\u00fck, C. et al. Selective coupling between theta phase and neocortical fast gamma oscillations during rem-sleep in mice. PLoS ONE 6, e28489 (2011).","journal-title":"PLoS ONE"},{"key":"29331_CR40","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.neuroscience.2009.08.047","volume":"164","author":"M Hunt","year":"2009","unstructured":"Hunt, M., Matulewicz, P., Gottesmann, C. & Kasicki, S. State-dependent changes in high-frequency oscillations recorded in the rat nucleus accumbens. Neurosci. 164, 380\u2013386 (2009).","journal-title":"Neurosci."},{"key":"29331_CR41","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1007\/s00213-013-3057-1","volume":"228","author":"SA Goda","year":"2013","unstructured":"Goda, S. A., Piasecka, J., Olszewski, M., Kasicki, S. & Hunt, M. J. Serotonergic hallucinogens differentially modify gamma and high frequency oscillations in the rat nucleus accumbens. Psychopharmacol. 228, 271\u2013282 (2013).","journal-title":"Psychopharmacol."},{"key":"29331_CR42","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/j.brainres.2010.09.088","volume":"1366","author":"P Matulewicz","year":"2010","unstructured":"Matulewicz, P., Kasicki, S. & Hunt, M. J. The effect of dopamine receptor blockade in the rodent nucleus accumbens on local field potential oscillations and motor activity in response to ketamine. Brain Res. 1366, 226\u2013232 (2010).","journal-title":"Brain Res."},{"key":"29331_CR43","doi-asserted-by":"publisher","first-page":"155","DOI":"10.3389\/fncir.2013.00155","volume":"7","author":"J L\u00f3pez-Azc\u00e1rate","year":"2013","unstructured":"L\u00f3pez-Azc\u00e1rate, J. et al. Delta-mediated cross-frequency coupling organizes oscillatory activity across the rat cortico-basal ganglia network. Front. Neural Circuits 7, 155 (2013).","journal-title":"Front. Neural Circuits"},{"key":"29331_CR44","doi-asserted-by":"crossref","unstructured":"D\u00fcrschmid, S. et al. Phase-amplitude cross-frequency coupling in the human nucleus accumbens tracks action monitoring during cognitive control. Front. Hum. Neurosci. 7 (2013).","DOI":"10.3389\/fnhum.2013.00635"},{"key":"29331_CR45","doi-asserted-by":"crossref","unstructured":"Terada, S., Takahashi, S. & Sakurai, Y. Oscillatory interaction between amygdala and hippocampus coordinates behavioral modulation based on reward expectation. Front. Behav. Neurosci. 7 (2013).","DOI":"10.3389\/fnbeh.2013.00177"},{"key":"29331_CR46","doi-asserted-by":"crossref","unstructured":"Andino-Pavlovsky, V. et al. Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats. Front. Neural Circuits 11 (2017).","DOI":"10.3389\/fncir.2017.00029"},{"key":"29331_CR47","doi-asserted-by":"publisher","first-page":"5338","DOI":"10.1523\/JNEUROSCI.3452-15.2016","volume":"36","author":"AL Lockmann","year":"2016","unstructured":"Lockmann, A. L., Laplagne, D. A., Le\u00e3o, R. N. & Tort, A. B. A respiration-coupled rhythm in the rat hippocampus independent of theta and slow oscillations. J. Neurosci. 36, 5338\u20135352 (2016).","journal-title":"J. Neurosci."},{"key":"29331_CR48","doi-asserted-by":"publisher","first-page":"45508","DOI":"10.1038\/srep45508","volume":"7","author":"J Biskamp","year":"2017","unstructured":"Biskamp, J., Bartos, M. & Sauer, J.-F. Organization of prefrontal network activity by respiration-related oscillations. Sci. Reports 7, 45508 (2017).","journal-title":"Sci. Reports"},{"key":"29331_CR49","doi-asserted-by":"crossref","unstructured":"Tort, A. B. et al. Parallel occurrence of theta and respiration-coupled network oscillations throughout the mouse brain. BioRxiv 139485 (2017).","DOI":"10.1101\/139485"},{"key":"29331_CR50","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00429-017-1573-1","volume":"223","author":"AL Lockmann","year":"2018","unstructured":"Lockmann, A. L. & Tort, A. B. Nasal respiration entrains delta-frequency oscillations in the prefrontal cortex and hippocampus of rodents. Brain Struct. Funct. 223, 1\u20133 (2018).","journal-title":"Brain Struct. Funct."},{"key":"29331_CR51","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. 114, 4519\u20134524 (2017).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"29331_CR52","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1017\/S146114571200106X","volume":"16","author":"P Belujon","year":"2013","unstructured":"Belujon, P., Patton, M. H. & Grace, A. A. Disruption of prefrontal cortical\u2013hippocampal balance in a developmental model of schizophrenia: reversal by sulpiride. Int. J. Neuropsychopharmacol. 16, 507\u2013512 (2013).","journal-title":"Int. J. Neuropsychopharmacol."},{"key":"29331_CR53","doi-asserted-by":"crossref","unstructured":"Gruber, A. J. & McDonald, R. J. Context, emotion, and the strategic pursuit of goals: interactions among multiple brain systems controlling motivated behavior. Front. Behav. Neurosci. 6 (2012).","DOI":"10.3389\/fnbeh.2012.00050"},{"key":"29331_CR54","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1093\/schbul\/sbr107","volume":"39","author":"A Anticevic","year":"2011","unstructured":"Anticevic, A., Repovs, G. & Barch, D. M. Working memory encoding and maintenance deficits in schizophrenia: neural evidence for activation and deactivation abnormalities. Schizophr. Bull. 39, 168\u2013178 (2011).","journal-title":"Schizophr. Bull."},{"key":"29331_CR55","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1016\/j.neuron.2012.09.016","volume":"76","author":"KG Phillips","year":"2012","unstructured":"Phillips, K. G. et al. Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76, 526\u2013533 (2012).","journal-title":"Neuron"},{"key":"29331_CR56","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1038\/npp.2014.184","volume":"40","author":"RJ Moran","year":"2015","unstructured":"Moran, R. J. et al. Losing control under ketamine: suppressed cortico-hippocampal drive following acute ketamine in rats. Neuropsychopharmacol. 40, 268 (2015).","journal-title":"Neuropsychopharmacol."},{"key":"29331_CR57","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1016\/j.bbr.2008.12.001","volume":"204","author":"SB Floresco","year":"2009","unstructured":"Floresco, S. B., Zhang, Y. & Enomoto, T. Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav. Brain Res. 204, 396\u2013409 (2009).","journal-title":"Behav. Brain Res."},{"key":"29331_CR58","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1093\/cercor\/bhs380","volume":"24","author":"P Belujon","year":"2012","unstructured":"Belujon, P., Patton, M. H. & Grace, A. A. Role of the prefrontal cortex in altered hippocampal\u2013accumbens synaptic plasticity in a developmental animal model of schizophrenia. Cereb. Cortex 24, 968\u2013977 (2012).","journal-title":"Cereb. Cortex"},{"key":"29331_CR59","doi-asserted-by":"publisher","first-page":"33","DOI":"10.3389\/neuro.09.033.2009","volume":"3","author":"KM Spencer","year":"2009","unstructured":"Spencer, K. M. The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling. Front. Hum. Neurosci. 3, 33 (2009).","journal-title":"Front. Hum. Neurosci."},{"key":"29331_CR60","doi-asserted-by":"publisher","first-page":"716","DOI":"10.1016\/j.biopsych.2015.07.005","volume":"79","author":"MP Jadi","year":"2016","unstructured":"Jadi, M. P., Behrens, M. M. & Sejnowski, T. J. Abnormal gamma oscillations in n-methyl-d-aspartate receptor hypofunction models of schizophrenia. Biol. Psychiatry 79, 716\u2013726 (2016).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR61","doi-asserted-by":"publisher","first-page":"17102","DOI":"10.1523\/JNEUROSCI.4623-10.2010","volume":"30","author":"AJ Gruber","year":"2010","unstructured":"Gruber, A. J. et al. More is less: a disinhibited prefrontal cortex impairs cognitive flexibility. J. Neurosci. 30, 17102\u201317110 (2010).","journal-title":"J. Neurosci."},{"key":"29331_CR62","doi-asserted-by":"publisher","first-page":"8977","DOI":"10.1523\/JNEUROSCI.1402-16.2016","volume":"36","author":"EC Zimmerman","year":"2016","unstructured":"Zimmerman, E. C. & Grace, A. A. The nucleus reuniens of the midline thalamus gates prefrontal-hippocampal modulation of ventral tegmental area dopamine neuron activity. J. Neurosci. 36, 8977\u20138984 (2016).","journal-title":"J. Neurosci."},{"key":"29331_CR63","doi-asserted-by":"crossref","unstructured":"Zhang, Y., Llinas, R. R. & Lisman, J. E. Inhibition of NMDARs in the nucleus reticularis of the thalamus produces delta frequency bursting. Front. Neural Circuits 3 (2009).","DOI":"10.3389\/neuro.04.020.2009"},{"key":"29331_CR64","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1017\/S1461145710000271","volume":"14","author":"T Kiss","year":"2011","unstructured":"Kiss, T., Hoffmann, W. E. & Haj\u00f3s, M. Delta oscillation and short-term plasticity in the rat medial prefrontal cortex: modelling NMDA hypofunction of schizophrenia. The Int. J. Neuropsychopharmacol. 14, 29\u201342 (2011).","journal-title":"The Int. J. Neuropsychopharmacol."},{"key":"29331_CR65","doi-asserted-by":"publisher","first-page":"3181","DOI":"10.1152\/jn.00072.2012","volume":"107","author":"Y Zhang","year":"2012","unstructured":"Zhang, Y., Yoshida, T., Katz, D. B. & Lisman, J. E. Nmdar antagonist action in thalamus imposes delta oscillations on the hippocampus. J. Neurophysiol. 107, 3181\u20133189 (2012).","journal-title":"J. Neurophysiol."},{"key":"29331_CR66","doi-asserted-by":"publisher","first-page":"e41908","DOI":"10.1371\/journal.pone.0041908","volume":"7","author":"Y Zhang","year":"2012","unstructured":"Zhang, Y., Buonanno, A., Vertes, R. P., Hoover, W. B. & Lisman, J. E. NR2C in the thalamic reticular nucleus; effects of the NR2C knockout. PLoS ONE 7, e41908 (2012).","journal-title":"PLoS ONE"},{"key":"29331_CR67","doi-asserted-by":"publisher","first-page":"1098","DOI":"10.1016\/j.biopsych.2015.01.020","volume":"77","author":"AR Duan","year":"2015","unstructured":"Duan, A. R. et al. Delta frequency optogenetic stimulation of the thalamic nucleus reuniens is sufficient to produce working memory deficits: relevance to schizophrenia. Biol. Psychiatry 77, 1098\u20131107 (2015).","journal-title":"Biol. Psychiatry"},{"key":"29331_CR68","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s00429-017-1587-8","volume":"223","author":"B Kocsis","year":"2018","unstructured":"Kocsis, B., Pittman-Polletta, B. R. & Roy, A. Respiration-coupled rhythms in prefrontal cortex: beyond if, to when, how, and why. Brain Struct. Funct. 223, 11\u201316 (2018).","journal-title":"Brain Struct. Funct."},{"key":"29331_CR69","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1038\/nrn.2016.57","volume":"17","author":"AA Grace","year":"2016","unstructured":"Grace, A. A. Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression. Nat. Rev. Neurosci. 17, 524 (2016).","journal-title":"Nat. Rev. Neurosci."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29331-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29331-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29331-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,21]],"date-time":"2022-12-21T02:57:10Z","timestamp":1671591430000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-018-29331-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,8,2]]},"references-count":69,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["29331"],"URL":"https:\/\/doi.org\/10.1038\/s41598-018-29331-8","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/191882","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,8,2]]},"assertion":[{"value":"2 October 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 June 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 August 2018","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":"11588"}}