{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T18:37:21Z","timestamp":1792089441801,"version":"4.4.0"},"reference-count":113,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,12,24]],"date-time":"2020-12-24T00:00:00Z","timestamp":1608768000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Sciences"],"abstract":"<jats:p>(1) Background. A one-time moderate hypobaric hypoxia (HBH) has a preconditioning effect whose neuronal mechanisms are not studied well. Previously, we found a stable correlation between the HBH efficiency and acoustic startle prepulse inhibition (PPI). This makes it possible to predict the individual efficiency of HBH in animals and to study its potential adaptive mechanisms. We revealed a bi-directional action of nicotinic \u03b17 receptor agonist PNU-282987 and its solvent dimethyl sulfoxide on HBH efficiency with the level of PPI &gt; or &lt; 40%. (2) The aim of the present study was to estimate cholinergic mechanisms of HBH effects in different brain regions. (3) Methods: in rats pretested for PPI, we evaluated the activity of synaptic membrane-bound and water-soluble choline acetyltransferase (ChAT) in the sub-fractions of \u2018light\u2019 and \u2018heavy\u2019 synaptosomes of the neocortex, hippocampus and caudal brainstem in the intact brain and after HBH. We tested the dose-dependent influence of PNU-282987 on the HBH efficiency. (4) Results: PPI level and ChAT activity correlated negatively in all brain structures of the intact animals, so that the values of the latter were higher in rats with PPI &lt; 40% compared to those with PPI &gt; 40%. After HBH, this ChAT activity difference was leveled in the neocortex and caudal brainstem, while for membrane-bound ChAT in the \u2018light\u2019 synaptosomal fraction of hippocampus, it was reversed to the opposite. In addition, a pharmacological study revealed that PNU-282987 in all used doses and its solvent displayed corresponding opposite effects on HBH efficiency in rats with different levels of PPI. (5) Conclusion: We substantiate that in rats with low and high PPI two opposite hippocampal cholinergic mechanisms are involved in hypoxic preconditioning, and both are implemented by forebrain projections via nicotinic \u03b17 receptors. Possible causes of association between general protective adaptation, HBH, PPI, forebrain cholinergic system and hippocampus are discussed.<\/jats:p>","DOI":"10.3390\/brainsci11010012","type":"journal-article","created":{"date-parts":[[2020,12,24]],"date-time":"2020-12-24T09:02:44Z","timestamp":1608800564000},"page":"12","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Opposite Pathways of Cholinergic Mechanisms of Hypoxic Preconditioning in the Hippocampus: Participation of Nicotinic \u03b17 Receptors and Their Association with the Baseline Level of Startle Prepulse Inhibition"],"prefix":"10.3390","volume":"11","author":[{"given":"Elena I.","family":"Zakharova","sequence":"first","affiliation":[{"name":"Laboratory of General Pathology of Cardiorespiratory System, Institute of General Pathology and Pathophysiology, Baltiyskaya, 8, 125315 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zinaida I.","family":"Storozheva","sequence":"additional","affiliation":[{"name":"Laboratory of Clinical Neurophysiology, Serbsky\u2019 National Medical Research Center for Psychiatry and Narcology, Kropotkinsky per., 23, 111395 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7258-7870","authenticated-orcid":false,"given":"Andrey T.","family":"Proshin","sequence":"additional","affiliation":[{"name":"Laboratory of Functional Neurochemistry, P.K. Anokhin Institute of Normal Physiology, Baltiyskaya, 8, 125315 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mikhail Yu.","family":"Monakov","sequence":"additional","affiliation":[{"name":"Laboratory of General Pathology of Cardiorespiratory System, Institute of General Pathology and Pathophysiology, Baltiyskaya, 8, 125315 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander M.","family":"Dudchenko","sequence":"additional","affiliation":[{"name":"Laboratory of General Pathology of Cardiorespiratory System, Institute of General Pathology and Pathophysiology, Baltiyskaya, 8, 125315 Moscow, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,12,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.pneurobio.2017.01.001","article-title":"Preconditioning in neuroprotection: From hypoxia to ischemia","volume":"157","author":"Li","year":"2017","journal-title":"Prog. Neurobiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"412","DOI":"10.4103\/aca.ACA_116_18","article-title":"Preconditioning in cardiac anesthesia\u2026\u2026 where are we?","volume":"22","author":"Annachhatre","year":"2019","journal-title":"Ann. Card. Anaesth."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1080\/19768354.2018.1557743","article-title":"Effects of hypoxic preconditioning on memory evaluated using the T-maze behavior test","volume":"23","author":"Kim","year":"2019","journal-title":"Anim. Cells Syst. (Seoul)"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1111\/wrr.12749","article-title":"A review on different methods to increase the efficiency of mesenchymal stem cell-based wound therapy","volume":"27","author":"Shojaei","year":"2019","journal-title":"Wound. Repair. Regen."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Zhang, W., Chen, M., Li, H., Yuan, J., Li, J., Wu, F., and Zhang, Y. (2019). Hypoxia preconditioning attenuates lung injury after thoracoscopic lobectomy in patients with lung cancer: A prospective randomized controlled trial. BMC Anesthesiol., 19.","DOI":"10.1186\/s12871-019-0854-z"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Sp\u00e4th, M.R., Koehler, F.C., Hoyer-Allo, K.J.R., Grundmann, F., Burst, V., and M\u00fcller, R.U. (2020). Preconditioning strategies to prevent acute kidney injury. F1000Res, 9.","DOI":"10.12688\/f1000research.21406.1"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1186\/s13287-020-01662-2","article-title":"Hypoxic preconditioning of human urine-derived stem cell-laden small intestinal submucosa enhances wound healing potential","volume":"11","author":"Zhang","year":"2020","journal-title":"Stem Cell Res. Ther."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/0006-8993(87)90571-3","article-title":"Dorsal and ventral respiratory groups of neurons in the medulla of the rat","volume":"419","author":"Saether","year":"1987","journal-title":"Brain Res."},{"key":"ref_9","first-page":"108","article-title":"Automatism or Rhythmogenesis in the Respiratory Center","volume":"29","author":"Safonov","year":"2003","journal-title":"Fiziol. Cheloveka."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2603","DOI":"10.1098\/rstb.2009.0082","article-title":"Chemosensory pathways in the brainstem controlling cardiorespiratory activity","volume":"364","author":"Spyer","year":"2009","journal-title":"Phil. Trans. R. Soc. B"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/B978-0-444-53825-3.00019-X","article-title":"Chapter 14\u2014Looking forward to breathing","volume":"188","author":"Feldman","year":"2011","journal-title":"Prog. Brain Res."},{"key":"ref_12","first-page":"58","article-title":"Respiratory rhythm generation in vivo","volume":"29","author":"Richter","year":"2014","journal-title":"Physiology (Bethesda)"},{"key":"ref_13","first-page":"206","article-title":"1975. Neural regulation of respiration","volume":"111","author":"Mitchell","year":"1975","journal-title":"Am. Rev. Respir. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1089\/brain.2015.0378","article-title":"The structural connectome of the human central homeostatic network","volume":"6","author":"Edlow","year":"2016","journal-title":"Brain Connect."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.neuroscience.2016.12.016","article-title":"Amygdalar and hippocampal connections with brainstem and spinal cord: A diffusion MRI study in human brain","volume":"343","author":"Arrigo","year":"2017","journal-title":"Neuroscience"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3389\/fnana.2017.00015","article-title":"The brainstem in emotion: A review","volume":"11","author":"Venkatraman","year":"2017","journal-title":"Front. Neuroanat."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/j.neuroimage.2019.01.060","article-title":"Multimodal Assessment of Recovery From Coma in a Rat Model of Diffuse Brainstem Tegmentum Injury","volume":"189","author":"Edlow","year":"2019","journal-title":"Neuroimage"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1097\/00001756-199502000-00038","article-title":"Alteration of [3H]hemicholinium-3 binding in the post-ischaemic gerbil brain","volume":"6","author":"Araki","year":"1995","journal-title":"Neuroreport"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1016\/j.resp.2015.01.014","article-title":"Respiratory neurobiology consortium. Facts and challenges in respiratory neurobiology","volume":"258","author":"Dick","year":"2018","journal-title":"Resp. Physiol. Neurobiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Das, K.K., and Biradar, M.S. (2018). Hypoxic Preconditioning: The multiplicity of central neurotransmitter mechanisms and method of predicting its efficiency. Hypoxia and Anoxia, InTechOPEN. Chapter 6.","DOI":"10.5772\/intechopen.73765"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1002\/iub.31","article-title":"Molecular Mechanism of Preconditioning","volume":"60","author":"Das","year":"2008","journal-title":"IUBMB Life"},{"key":"ref_22","first-page":"32","article-title":"Efficiency and mechanism for different regimens of hypoxic training: The possibility of optimization of hypoxic therapy","volume":"6","author":"Lukyanova","year":"2008","journal-title":"Pathogenesis"},{"key":"ref_23","first-page":"51","article-title":"Effect of hypoxia on dynamics of HIF-1alpha level in the cerebral cortex and development of adaptation in rats with different resistance to hypoxia","volume":"56","author":"Kirova","year":"2012","journal-title":"Patol. Fiziol. Eksp. Ter."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1023\/A:1015828227115","article-title":"Comparison of the cholinergic system in neocortical field Ep in cats with strong and weak cognitive abilities","volume":"32","author":"Mukhin","year":"2002","journal-title":"Neurosci. Behav. Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1134\/S1819712410040082","article-title":"Cholinergic Systems of the Rat Brain and Neuronal Reorganization under Conditions of Acute Hypoxia","volume":"4","author":"Zakharova","year":"2010","journal-title":"Neurochem. J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1134\/S1819712413010108","article-title":"Central Cholinergic Systems in the Mechanisms of Hypoxic Preconditioning: Diverse Pathways of Synaptic Reorganization in Vivo","volume":"7","author":"Zakharova","year":"2013","journal-title":"Neurochem. J."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Zakharova, E.I., Storozheva, Z.I., Dudchenko, A.M., and Kubatiev, A.A. (2010). Chronic cereral ischemia forms news mechanisms of learning and memory. Int. J. Alzheimers Dis., 1\u201317.","DOI":"10.4061\/2010\/954589"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Heinbockel, T. (2014). Synaptic soluble and membrane-bound choline acetyltransferase as a marker of cholinergic function in vitro and in vivo. Neurochemistry, InTechOpen. Chapter 5.","DOI":"10.5772\/57074"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/0006-8993(86)90010-7","article-title":"Veratridine-induced breakdown of 11 cytosolic acetylcholine in rat hippocampal minces: An intraterminal form of acetyl-12 cholinesterase or choline O-acetyltransferase?","volume":"383","author":"Carrol","year":"1986","journal-title":"Brain Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/S0079-6123(08)62394-8","article-title":"Regulation of the synthesis of acetylcholine","volume":"98","author":"Rylett","year":"1993","journal-title":"Prog. Braim Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0006-8993(96)01485-0","article-title":"Evidence to suggest that extracellular acetate is accumulated by rat hippocampal cholinergic nerve terminals for acetylcholine formation and release","volume":"753","author":"Carroll","year":"1997","journal-title":"Brain Res."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1046\/j.1460-9568.1999.00571.x","article-title":"Acetylcho\u201414 line synthesis and quantal release reconstituted by transfection of mediatophore and 15 choline acetyltranferase cDNAs","volume":"11","author":"Bloc","year":"1999","journal-title":"Eur. J. Neurosci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1023\/B:NERE.0000010449.05927.f9","article-title":"Choline acetyltransferase: Regulation and coupling with protein kinase and vesicular acetylcholine transporter on synaptic vesicles","volume":"29","author":"Sha","year":"2004","journal-title":"Neurochem. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"563","DOI":"10.4236\/jbise.2016.912049","article-title":"Hypoxic Preconditioning Eliminates Differences in the Innate Resistance of Rats to Severe Hypoxia","volume":"9","author":"Zakharova","year":"2016","journal-title":"J. Biomed. Sci. Eng."},{"key":"ref_35","unstructured":"Dudchenko, A.M., Zakharova, E.I., and Storozheva, Z.I. (2014). Method for Predicting the Limit of Resistance of Animals to Severe Hypoxia after Hypoxic Preconditioning. (2571603), RU Patent."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s00213-008-1072-4","article-title":"Realistic expectations of prepulse inhibition in translational models for schizophrenia research","volume":"199","author":"Swerdlow","year":"2008","journal-title":"Psychopharmacology"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"15262","DOI":"10.1523\/JNEUROSCI.0160-12.2012","article-title":"Axonal conduction block as a novel mechanism of prepulse inhibition","volume":"32","author":"Lee","year":"2012","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"G\u00f3mez-Nieto, R., Hormigo, S., and L\u00f3pez, D.E. (2020). Prepulse Inhibition of the Auditory Startle Reflex Assessment as a Hallmark of Sensorimotor Gating Mechanisms. Brain Sci., 10.","DOI":"10.20944\/preprints202008.0356.v1"},{"key":"ref_39","first-page":"525","article-title":"Dynamics of Defensive Response Mobilization to Approaching External Versus Interoceptive Threat","volume":"3","author":"Krause","year":"2018","journal-title":"Biol. Psychiatry Cogn. Neurosci. Neuroimaging"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/S0006-8993(97)00194-7","article-title":"Nicotinic alpha 7 receptors protect against glutamate neurotoxicity and neuronal ischemic damage","volume":"779","author":"Shimohama","year":"1998","journal-title":"Brain Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/j.jneumeth.2008.10.012","article-title":"A new model for the study of high-K(+)-induced preconditioning in cultured neurones: Role of N-methyl-d-aspartate and alpha7-nicotinic acetylcholine receptors","volume":"177","author":"Errington","year":"2009","journal-title":"J. Neurosci. Methods"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1111\/jnc.13097","article-title":"miR-210 Mediates Vagus Nerve Stimulation-Induced Antioxidant Stress and Anti-Apoptosis Reactions Following Cerebral Ischemia\/Reperfusion Injury in Rats","volume":"134","author":"Jiang","year":"2015","journal-title":"J. Neurochem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/s10020-019-0091-4","article-title":"Electroacupuncture attenuated cerebral ischemic injury and neuroinflammation through \u03b17nAChR-mediated inhibition of NLRP3 inflammasome in stroke rats","volume":"25","author":"Jiang","year":"2019","journal-title":"Mol. Med."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2045","DOI":"10.1007\/s12035-016-9796-3","article-title":"Boosting Endogenous Resistance of Brain to Ischemia","volume":"54","author":"Sun","year":"2017","journal-title":"Mol. Neurobiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"10","DOI":"10.4236\/jbise.2018.111002","article-title":"The Acoustic Sensorimotor Gating Predicts the Efficiency of Hypoxic Preconditioning. Participation of the Cholinergic System in This Phenomenon","volume":"11","author":"Zakharova","year":"2018","journal-title":"J. Biomed. Sci. Eng."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1038\/212405a0","article-title":"Cholinesterase inhibitory property of dimethyl sulphoxide","volume":"212","author":"Sams","year":"1966","journal-title":"Nature"},{"key":"ref_47","first-page":"1455","article-title":"Diversity of nicotinic acetylcholine receptors in rat hippocampal neurons: I. Pharmacological and functional evidence for distinct structural subtypes","volume":"265","author":"Alkondon","year":"1993","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1124\/jpet.104.076968","article-title":"The selective alpha7 nicotinic acetylcholine receptor agonist PNU-282987 [N-[(3R)-1-Azabicyclo [2.2.2]oct-3-yl]-4-chlorobenzamide hydrochloride] enhances GABAergic synaptic activity in brain slices and restores auditory gating deficits in anesthetized rats","volume":"312","author":"Hurst","year":"2005","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.bcp.2015.07.006","article-title":"Concentration-response relationship of the \u03b17 nicotinic acetylcholine receptor agonist FRM-17874 across multiple in vitro and in vivo assays","volume":"97","author":"Stoiljkovic","year":"2015","journal-title":"Biochem. Pharmacol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"7993","DOI":"10.1523\/JNEUROSCI.21-20-07993.2001","article-title":"Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus","volume":"21","author":"Skehel","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1016\/j.bcp.2011.04.019","article-title":"An autoradiographic survey of mouse brain nicotinic acetylcholine receptors defined by null mutants","volume":"82","author":"Baddick","year":"2011","journal-title":"Biochem. Pharmacol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1007\/s10517-016-3183-y","article-title":"A Hardware-and-Software System for Experimental Studies of the Acoustic Startle Response in Laboratory Rodents","volume":"160","author":"Pevtsov","year":"2016","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1111\/j.1471-4159.1962.tb07489.x","article-title":"Cholinergic and non-cholinergic nerve endings in rat brain. I. Isolation and subcellular distribution of acetylcholine and acetylcholinesterase","volume":"9","author":"Salganicoff","year":"1962","journal-title":"J. Neurochem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1016\/0005-2736(71)90117-9","article-title":"Synaptic plasma membranes from rat brain synaptosomes: Isolation and partial characterization","volume":"249","author":"Cotman","year":"1971","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_55","first-page":"88","article-title":"Ultrastructural and biochemical characterization of the subfractions of synaptic membranes isolated from light and heavy synaptosomes of the brain","volume":"89","author":"Bogolepov","year":"1985","journal-title":"Arkh. Anat. Gistol. Embriol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1042\/bj1150465","article-title":"Radiochemical microassays for the determination of choline acetyltransferase and acetylcholinesterase activities","volume":"115","author":"Fonnum","year":"1969","journal-title":"Biochem. J."},{"key":"ref_57","unstructured":"Kobzar, A.I. (2006). Applied Mathematical Statistics. For Engineers and Scientists, FIZMATLIT."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/S0306-4522(01)00413-4","article-title":"Selective Immunolesioning of Cholinergic Neurons in Nucleus Basalis Magnocellularis Impairs Prepulse Inhibition of Acoustic Startle","volume":"108","author":"Ballmaier","year":"2001","journal-title":"Neuroscience"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1152\/jn.01119.2006","article-title":"Strain-specific nicotinic modulation of glutamatergic transmission in the CA1 field of the rat hippocampus: August Copenhagen Irish versus Sprague-Dawley","volume":"97","author":"Alkondon","year":"2007","journal-title":"J. Neurophysiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.bbr.2013.06.030","article-title":"Loss of rostral brainstem cholinergic activity results in decreased ultrasonic vocalization behavior and altered sensorimotor gating","volume":"256","author":"Machold","year":"2013","journal-title":"Behav. Brain Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"8798","DOI":"10.1523\/JNEUROSCI.0984-18.2018","article-title":"The Role of Cholinergic Midbrain Neurons in Startle and Prepulse Inhibition","volume":"38","author":"Azzopardi","year":"2018","journal-title":"J. Neurosci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1007\/s00213-001-0927-8","article-title":"Effects of alpha 4\/beta 2- and alpha 7-nicotine acetylcholine receptor agonists on prepulse inhibition of the acoustic startle response in rats and mice","volume":"159","author":"Schreiber","year":"2002","journal-title":"Psychopharmacology"},{"key":"ref_63","first-page":"54","article-title":"Varenicline disrupts prepulse inhibition only in high-inhibitory rats. Prog. Neuropsychopharmacol","volume":"53","author":"Goktalay","year":"2014","journal-title":"Biol. Psychiatry"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.neulet.2014.03.070","article-title":"CDP-choline attenuates scopolamine induced disruption of prepulse inhibition in rats: Involvement of central nicotinic mechanism","volume":"569","author":"Uslu","year":"2014","journal-title":"Neurosci. Lett."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/0006-8993(87)90024-2","article-title":"Veratridine-induced activation of choline-O-acetyltransferase activity in rat hippocampal tissue: Relationship to the veratridine-induced release of acetylcholine","volume":"414","author":"Carroll","year":"1987","journal-title":"Brain Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1774","DOI":"10.1111\/j.1471-4159.1993.tb09815.x","article-title":"Phosphorylation of rat brain choline acetyltransferase and its relationship to enzyme activity","volume":"61","author":"Schmidt","year":"1993","journal-title":"J. Nerochem."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0006-8993(93)91367-2","article-title":"Membrane-bound choline-O-acetyltransferase in rat hippocampal tissue is anchored by glycosyl-phosphatidylinositol","volume":"605","author":"Smith","year":"1993","journal-title":"Brain Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1113\/jphysiol.2010.199224","article-title":"Synaptic vesicles control the time course of neurotransmitter secretion via a Ca\u00b2+\/H+ antiport","volume":"589","author":"Cordeiro","year":"2011","journal-title":"J. Physiol."},{"key":"ref_69","first-page":"569","article-title":"Synaptosomal uptake of choline and of gamma-aminobutyric acid: Effects of ethanol and of dimethylsulfoxide","volume":"10","author":"North","year":"1989","journal-title":"Neurotoxicology"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/0304-3940(92)90459-K","article-title":"Dimethyl sulfoxide (DMSO) blocks GABA-induced current in rat dorsal root ganglion neurons","volume":"138","author":"Nakahiro","year":"1992","journal-title":"Neurosci. Lett."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0304-3940(97)00505-3","article-title":"Differential Effects of Dimethyl Sulfoxide on Nicotinic Acetylcholine Receptors from Mouse Muscle and Torpedo Electrocytes","volume":"230","author":"Eaton","year":"1997","journal-title":"Neurosci. Lett."},{"key":"ref_72","first-page":"213","article-title":"Effects of Dimethyl Sulfoxide on Neuronal Response Characteristics in Deep Layers of Rat Barrel Cortex","volume":"7","author":"Soltani","year":"2016","journal-title":"Basic Clin. Neurosci."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1712","DOI":"10.1038\/s41386-018-0066-0","article-title":"Nicotinic receptor-modulating agents reverse the hyperdopaminergic tone in the MAM model of schizophrenia","volume":"43","author":"Neves","year":"2018","journal-title":"Neuropsychopharmacology"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.neuropharm.2016.02.008","article-title":"Activation of \u03b17 nicotinic acetylcholine receptors protects potentiated synapses from depotentiation during theta pattern stimulation in the hippocampal CA1 region of rats","volume":"105","author":"Galvez","year":"2016","journal-title":"Neuropharmacology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1002\/hipo.1073","article-title":"Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information","volume":"11","author":"Vinogradova","year":"2001","journal-title":"Hippocampus"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1016\/j.neuron.2005.05.002","article-title":"The hippocampal-VTA loop: Controlling the entry of information into long-term memory","volume":"46","author":"Lisman","year":"2005","journal-title":"Neuron"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"19537","DOI":"10.1073\/pnas.1008638107","article-title":"Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory","volume":"107","author":"Wang","year":"2010","journal-title":"PNAS"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nature19325","article-title":"Locus coeruleus and dopaminergic consolidation of everyday memory","volume":"537","author":"Takeuchi","year":"2016","journal-title":"Nature"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1002\/hipo.23020","article-title":"Temporal coding and rate remapping: Representation of nonspatial information in the hippocampus","volume":"29","author":"Sanders","year":"2019","journal-title":"Hippocampus"},{"key":"ref_80","first-page":"5045","article-title":"Intermediate-Term Memory as a Bridge between Working and Long-Term Memory","volume":"17","year":"2017","journal-title":"J. Neurosci."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1007\/s10517-005-0466-0","article-title":"Adaptation to periodic hypoxia and hyperoxia improves resistance of membrane structures in heart, liver, and brain","volume":"140","author":"Arkhipenko","year":"2005","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_82","first-page":"26","article-title":"Vasoprotective effect of adaptation to hypoxia in myocardial ischemia and reperfusion injury","volume":"57","author":"Manukhina","year":"2013","journal-title":"Patol. Fiziol. Eksp. Ter."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"388","DOI":"10.3389\/fnins.2015.00388","article-title":"Current insights into the molecular mechanisms of hypoxic pre- and postconditioning using hypobaric hypoxia","volume":"9","author":"Rybnikova","year":"2015","journal-title":"Front. Neurosci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1708","DOI":"10.1177\/1535370216657614","article-title":"Intermittent hypoxia training as non-pharmacologic therapy for cardiovascular diseases: Practical analysis on methods and equipment","volume":"241","author":"Serebrovskaya","year":"2016","journal-title":"Exp. Biol. Med."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1007\/s11064-018-2593-9","article-title":"Nitric Oxide Participates in the Brain Ischemic Tolerance Induced by Intermittent Hypobaric Hypoxia in the Hippocampal CA1 Subfield in Rats","volume":"43","author":"Huang","year":"2018","journal-title":"Neurochem. Res."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"770","DOI":"10.3389\/fnins.2019.00770","article-title":"Editorial: Brain Hypoxia and Ischemia: New Insights Into Neurodegeneration and Neuroprotection","volume":"13","author":"Nalivaeva","year":"2019","journal-title":"Front. Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.resp.2018.03.004","article-title":"Hippocampal modulation of cardiorespiratory function","volume":"252\u2013253","author":"Ajayi","year":"2018","journal-title":"Respir. Physiol. Neurobiol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1016\/0306-4522(93)90484-W","article-title":"Acetylcholine, theta-rhythm and activity of hippocampal neurons in the rabbit-IV Sensorystimulation","volume":"53","author":"Vinogradova","year":"1993","journal-title":"Neuroscience"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"13535","DOI":"10.1073\/pnas.1411233111","article-title":"Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus","volume":"111","author":"Vandecasteele","year":"2014","journal-title":"PNAS"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1007\/s00441-017-2745-2","article-title":"Septo-hippocampal interaction","volume":"373","author":"Remy","year":"2018","journal-title":"Cell Tissue Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1016\/S0736-5748(98)00073-2","article-title":"Immunolesion of the cholinergic basal forebrain: Effects on functional properties of hippocampal and septal neurons","volume":"16","author":"Bassant","year":"1998","journal-title":"Int. J. Dev. Neurosci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1016\/j.celrep.2017.07.053","article-title":"NKX2-1 Is Required in the Embryonic Septum for Cholinergic System Development, Learning, and Memory","volume":"20","author":"Magno","year":"2017","journal-title":"Cell Rep."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1111\/nan.12513","article-title":"Revisiting the human cholinergic nucleus of the diagonal band of Broca. Neuropathol","volume":"44","author":"Liu","year":"2018","journal-title":"Appl. Neurobiol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"2199","DOI":"10.1111\/ejn.14089","article-title":"Cholinergic modulation of spatial learning, memory and navigation","volume":"48","author":"Solari","year":"2018","journal-title":"Eur. J. Neurosci."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1002\/hipo.20136","article-title":"Medial septal modulation of the ascending brainstem hippocampal synchronizing pathways in the freely moving rat","volume":"16","author":"Bland","year":"2006","journal-title":"Hippocampus"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1152\/physrev.00015.2008","article-title":"Mammalian nicotinic acetylcholine receptors: From structure to function","volume":"89","author":"Albuquerque","year":"2009","journal-title":"Physiol. Rev."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0896-6273(01)00332-4","article-title":"Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity","volume":"31","author":"Ji","year":"2001","journal-title":"Neuron"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.neuropharm.2016.02.028","article-title":"Integration of inhibitory and excitatory effects of \u03b17 nicotinic acetylcholine receptor activation in the prelimbic cortex regulates network activity and plasticity","volume":"105","author":"Udakis","year":"2016","journal-title":"Neuropharmacology"},{"key":"ref_99","doi-asserted-by":"crossref","unstructured":"Hummos, A., and Nair, S.S. (2017). An integrative model of the intrinsic hippocampal theta rhythm. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0182648"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1267","DOI":"10.1038\/npp.2017.276","article-title":"Bidirectional Regulation of Aggression in Mice by Hippocampal Alpha- 7 Nicotinic Acetylcholine Receptors","volume":"43","author":"Lewis","year":"2018","journal-title":"Neuropsychopharmacology"},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Benfante, R., Di Lascio, S., Cardani, S., and Fornasari, D. (2019). Acetylcholinesterase inhibitors targeting the cholinergic anti-inflammatory pathway: A new therapeutic perspective in aging-related disorders. Aging Clin. Exp. Res., 1\u201312.","DOI":"10.1007\/s40520-019-01359-4"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1177\/2398212818771821","article-title":"The dynamics of disordered dialogue: Prefrontal, hippocampal and thalamic miscommunication underlying working memory deficits in schizophrenia","volume":"2","author":"Kupferschmidt","year":"2018","journal-title":"Brain Neurosci. Adv."},{"key":"ref_103","first-page":"13","article-title":"The specificity of cholinergic mechanisms of learning and memory in rats with different levels of ability for spatial contextual learning in the Morris water maze","volume":"62","author":"Zakharova","year":"2018","journal-title":"Patol. Fiziol. Eksp. Ter."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fnsyn.2015.00004","article-title":"Hippocampal \u201ccholinergic interneurons\u201d visualized with the choline acetyltransferase promoter: Anatomical distribution, intrinsic membrane properties, neurochemical characteristics, and capacity for cholinergic modulation","volume":"7","author":"Yi","year":"2015","journal-title":"Front. Synaptic Neurosci."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.jphysparis.2011.09.007","article-title":"Neural circuits underlying the generation of theta oscillations","volume":"106","author":"Pignatelli","year":"2012","journal-title":"J. Physiol. Paris"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"5234","DOI":"10.1523\/JNEUROSCI.0950-18.2019","article-title":"Cholinergic Neurons of the Medial Septum Are Crucial for Sensorimotor Gating","volume":"39","author":"Jin","year":"2019","journal-title":"J. Neurosci."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"R1008","DOI":"10.1152\/ajpregu.00075.2002","article-title":"In vivo electrophysiological responses of pedunculopontine neurons to static muscle contraction","volume":"283","author":"Plowey","year":"2002","journal-title":"Am. J. Physiol. Regul Integr. Comp. Physiol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/0361-9230(86)90134-6","article-title":"Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain","volume":"16","author":"Woolf","year":"1986","journal-title":"Brain Res. Bull."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1002\/cne.902670311","article-title":"Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat","volume":"267","author":"Semba","year":"1988","journal-title":"J. Comp. Neurol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1016\/0361-9230(89)90197-4","article-title":"Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum","volume":"23","author":"Woolf","year":"1989","journal-title":"Brain Res. Bull."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1016\/0361-9230(89)90102-0","article-title":"Brainstem projecting neurons in the rat basal forebrain: Neurochemical, topographical, and physiological distinctions from cortically projecting cholinergic neurons","volume":"22","author":"Semba","year":"1989","journal-title":"Brain Res. Bull."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.bbr.2018.12.033","article-title":"Volumetric brain differences between the Roman rat strains: Neonatal handling effects, sensorimotor gating and working memory","volume":"361","author":"Piludu","year":"2019","journal-title":"Behav. Brain Res."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"447","DOI":"10.55782\/ane-2007-1661","article-title":"Modulation of hippocampal theta rhythm by the opioid system of the pedunculopontine tegmental nucleus","volume":"67","author":"Leszkowicz","year":"2007","journal-title":"Acta Neurobiol. Exp. (Wars)"}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/11\/1\/12\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:45:35Z","timestamp":1760179535000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/11\/1\/12"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,24]]},"references-count":113,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["brainsci11010012"],"URL":"https:\/\/doi.org\/10.3390\/brainsci11010012","relation":{},"ISSN":["2076-3425"],"issn-type":[{"value":"2076-3425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,24]]}}}