{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,30]],"date-time":"2026-04-30T16:06:59Z","timestamp":1777565219004,"version":"3.51.4"},"reference-count":66,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2022,4,20]],"date-time":"2022-04-20T00:00:00Z","timestamp":1650412800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["FCT UIDB\/04046\/2020"],"award-info":[{"award-number":["FCT UIDB\/04046\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["UIDP\/04046\/2020"],"award-info":[{"award-number":["UIDP\/04046\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/SAU-NEU\/103639\/2008"],"award-info":[{"award-number":["PTDC\/SAU-NEU\/103639\/2008"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/SAU-PUB\/28311\/2017"],"award-info":[{"award-number":["PTDC\/SAU-PUB\/28311\/2017"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/81358\/2011"],"award-info":[{"award-number":["SFRH\/BPD\/81358\/2011"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["DL57\/2016\/CP1479\/CT0044"],"award-info":[{"award-number":["DL57\/2016\/CP1479\/CT0044"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Vasoactive intestinal peptide (VIP), acting on both VPAC1 and VPAC2 receptors, is a key modulator of hippocampal synaptic transmission, pyramidal cell excitability and long-term depression (LTD), exerting its effects partly through modulation GABAergic disinhibitory circuits. Yet, the role of endogenous VIP and its receptors in modulation of hippocampal LTP and the involvement of disinhibition in this modulation have scarcely been investigated. We studied the modulation of CA1 LTP induced by TBS via endogenous VIP release in hippocampal slices from young-adult Wistar rats using selective VPAC1 and VPAC2 receptor antagonists, evaluating its consequence for the phosphorylation of CamKII, GluA1 AMPA receptor subunits and Kv4.2 potassium channels in total hippocampal membranes obtained from TBS stimulated slices. Endogenous VIP, acting on VPAC1 (but not VPAC2) receptors, inhibited CA1 hippocampal LTP induced by TBS in young adult Wistar rats and this effect was dependent on GABAergic transmission and relied on the integrity of NMDA and CaMKII-dependent LTP expression mechanisms but not on PKA and PKC activity. Furthermore, it regulated the autophosphorylation of CaMKII and the expression and Ser438 phosphorylation of Kv4.2 potassium channels responsible for the A-current while inhibiting phosphorylation of Kv4.2 on Thr607. Altogether, this suggests that endogenous VIP controls the expression of hippocampal CA1 LTP by regulating disinhibition through activation of VPAC1 receptors in interneurons. This may impact the autophosphorylation of CaMKII during LTP, as well as the expression and phosphorylation of Kv4.2 K+ channels at hippocampal pyramidal cell dendrites.<\/jats:p>","DOI":"10.3390\/biology11050627","type":"journal-article","created":{"date-parts":[[2022,4,21]],"date-time":"2022-04-21T01:55:51Z","timestamp":1650506151000},"page":"627","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Endogenous VIP VPAC1 Receptor Activation Modulates Hippocampal Theta Burst Induced LTP: Transduction Pathways and GABAergic Mechanisms"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4051-5952","authenticated-orcid":false,"given":"Ana","family":"Caulino-Rocha","sequence":"first","affiliation":[{"name":"Departamento de Qu\u00edmica e Bioqu\u00edmica Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"},{"name":"BioISI\u2014Instituto de Biosistemas e Ci\u00eancias Integrativas, Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"N\u00e1dia Carolina","family":"Rodrigues","sequence":"additional","affiliation":[{"name":"Unidade de Neuroci\u00eancias, Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9330-3507","authenticated-orcid":false,"given":"Joaquim Alexandre","family":"Ribeiro","sequence":"additional","affiliation":[{"name":"Unidade de Neuroci\u00eancias, Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, Portugal"},{"name":"Instituto de Farmacologia e Neuroci\u00eancias, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0900-9306","authenticated-orcid":false,"given":"Diana","family":"Cunha-Reis","sequence":"additional","affiliation":[{"name":"Departamento de Qu\u00edmica e Bioqu\u00edmica Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"},{"name":"BioISI\u2014Instituto de Biosistemas e Ci\u00eancias Integrativas, Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"},{"name":"Unidade de Neuroci\u00eancias, Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Av. Prof. Egas Moniz, 1649-028 Lisboa, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"153","DOI":"10.3389\/fncel.2020.00153","article-title":"VIP Modulation of Hippocampal Synaptic Plasticity: A Role for VIP Receptors as Therapeutic Targets in Cognitive Decline and Mesial Temporal Lobe Epilepsy","volume":"14","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1101\/lm.40501","article-title":"Differential Effects of PACAP-38 on Synaptic Responses in Rat Hippocampal CA1 Region","volume":"8","author":"Roberto","year":"2001","journal-title":"Learn. Mem."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/0306-4522(95)00610-9","article-title":"Correlated Morphological and Neurochemical Features Identify Different Subsets of Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons in Rat Hippocampus","volume":"73","author":"Arabadzisz","year":"1996","journal-title":"Neuroscience"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1016\/S0006-8993(96)00772-X","article-title":"Vasoactive Intestinal Polypeptide Enhances the GABAergic Synaptic Transmission in Cultured Hippocampal Neurons","volume":"746","author":"Wang","year":"1997","journal-title":"Brain Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"4725","DOI":"10.1111\/bph.14051","article-title":"VPAC1 and VPAC2 Receptor Activation on GABA Release from Hippocampal Nerve Terminals Involve Several Different Signalling Pathways","volume":"174","author":"Ribeiro","year":"2017","journal-title":"Br. J. Pharmacol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1002\/cne.20231","article-title":"Distribution of Vasoactive Intestinal Peptide and Pituitary Adenylate Cyclase-Activating Polypeptide Receptors (VPAC1, VPAC2, and PAC1 Receptor) in the Rat Brain","volume":"476","author":"Joo","year":"2004","journal-title":"J. Comp. Neurol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1016\/S0196-9781(97)00229-5","article-title":"Autoradiographic Visualization of the Receptor Subclasses for Vasoactive Intestinal Polypeptide (VIP) in Rat Brain","volume":"18","author":"Vertongen","year":"1997","journal-title":"Peptides"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1016\/S0014-4886(03)00300-5","article-title":"Opposing Effects by Pituitary Adenylate Cyclase-Activating Polypeptide and Vasoactive Intestinal Peptide on Hippocampal Synaptic Transmission","volume":"184","author":"Ciranna","year":"2003","journal-title":"Exp. Neurol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/0306-4522(92)90243-U","article-title":"Vasoactive Intestinal Polypeptide Modulates Neuronal Excitability in Hippocampal Slices of the Rat","volume":"47","author":"Haas","year":"1992","journal-title":"Neuroscience"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1139\/y94-005","article-title":"Impaired Spatial Learning by Vasoactive Intestinal Peptide in Morris Water Maze Task in the Rat","volume":"72","author":"Itoh","year":"1994","journal-title":"Can. J. Physiol. Pharmacol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.regpep.2009.05.009","article-title":"Lateralized Learning and Memory Effects of Vasoactive Intestinal Peptide Infused into the Rat Hippocampal CA1 Area","volume":"156","author":"Ivanova","year":"2009","journal-title":"Regul. Pept."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1016\/0196-9781(93)90089-Y","article-title":"Influence of Chronic Intracerebroventricular Infusion of Vasoactive Intestinal Peptide (VIP) on Memory Processes in Morris Water Pool Test in the Rat","volume":"14","author":"Takashima","year":"1993","journal-title":"Peptides"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1016\/0196-9781(93)90088-X","article-title":"Vasoactive Intestinal Peptide (VIP) Causes Memory Impairment in Passive Avoidance Responding of the Rat","volume":"14","author":"Takashima","year":"1993","journal-title":"Peptides"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1150","DOI":"10.1016\/j.neuron.2019.01.009","article-title":"Vasoactive Intestinal Polypeptide-Expressing Interneurons in the Hippocampus Support Goal-Oriented Spatial Learning","volume":"101","author":"Turi","year":"2019","journal-title":"Neuron"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.expneurol.2008.01.003","article-title":"Deficits in Social Behavior and Reversal Learning Are More Prevalent in Male Offspring of VIP Deficient Female Mice","volume":"211","author":"Stack","year":"2008","journal-title":"Exp. Neurol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1002\/hipo.22316","article-title":"Endogenous Inhibition of Hippocampal LTD and Depotentiation by Vasoactive Intestinal Peptide VPAC1 Receptors","volume":"24","author":"Ribeiro","year":"2014","journal-title":"Hippocampus"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1002\/hipo.20559","article-title":"Vasoactive Intestinal Peptide Acts via Multiple Signal Pathways to Regulate Hippocampal NMDA Receptors and Synaptic Transmission","volume":"19","author":"Yang","year":"2009","journal-title":"Hippocampus"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.nlm.2017.09.004","article-title":"Mismatch Novelty Exploration Training Enhances Hippocampal Synaptic Plasticity: A Tool for Cognitive Stimulation?","volume":"145","author":"Carmo","year":"2017","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/0006-8993(88)91388-1","article-title":"Role of N-Methyl-D-Aspartate Receptors in the Induction of Synaptic Potentiation by Burst Stimulation Patterned after the Hippocampal Theta-Rhythm","volume":"441","author":"Larson","year":"1988","journal-title":"Brain Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/0304-3940(86)90487-8","article-title":"Induction of Hippocampal Long-Term Potentiation Using Physiologically Patterned Stimulation","volume":"69","author":"Rose","year":"1986","journal-title":"Neurosci. Lett."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.brainres.2014.10.034","article-title":"Theta-Burst LTP","volume":"1621","author":"Larson","year":"2015","journal-title":"Brain Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1002\/hipo.20118","article-title":"Hippocampal Theta Rhythm: A Tag for Short-Term Memory","volume":"15","author":"Vertes","year":"2005","journal-title":"Hippocampus"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1113\/jphysiol.1990.sp018080","article-title":"Paired-Pulse Depression of Monosynaptic GABA-Mediated Inhibitory Postsynaptic Responses in Rat Hippocampus","volume":"424","author":"Davies","year":"1990","journal-title":"J. Physiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/0006-8993(86)90579-2","article-title":"Patterned Stimulation at the Theta Frequency Is Optimal for the Induction of Hippocampal Long-Term Potentiation","volume":"368","author":"Larson","year":"1986","journal-title":"Brain Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1113\/jphysiol.1996.sp021698","article-title":"Regulation of EPSPs by the Synaptic Activation of GABA(B) Autoreceptors in Rat Hippocampus","volume":"496","author":"Davies","year":"1996","journal-title":"J. Physiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"5272","DOI":"10.1111\/ejn.15390","article-title":"Hippocampal CA1 Theta Burst-Induced LTP from Weaning to Adulthood: Cellular and Molecular Mechanisms in Young Male Rats Revisited","volume":"54","author":"Rodrigues","year":"2021","journal-title":"Eur. J. Neurosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/S0165-0270(01)00374-0","article-title":"The LTP Program: A Data Acquisition Program for on-Line Analysis of Long-Term Potentiation and Other Synaptic Events","volume":"108","author":"Anderson","year":"2001","journal-title":"J. Neurosci. Methods"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1555","DOI":"10.1016\/S0196-9781(97)00230-1","article-title":"In Vitro Properties of a High Affinity Selective Antagonist of the VIP1 Receptor","volume":"18","author":"Gourlet","year":"1997","journal-title":"Peptides"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1543","DOI":"10.1016\/S0196-9781(00)00309-0","article-title":"Development of Selective Agonists and Antagonists for the Human Vasoactive Intestinal Polypeptide VPAC(2) Receptor","volume":"21","author":"Moreno","year":"2000","journal-title":"Peptides"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1111\/j.1471-4159.2010.07133.x","article-title":"LTP in Hippocampal Neurons Is Associated with a CaMKII-Mediated Increase in GluA1 Surface Expression","volume":"116","author":"Appleby","year":"2011","journal-title":"J. Neurochem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1113\/jphysiol.2006.111559","article-title":"Autophosphorylation of ACaMKII Is Not a General Requirement for NMDA Receptor-Dependent LTP in the Adult Mouse","volume":"574","author":"Cooke","year":"2006","journal-title":"J. Physiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1016\/S0092-8674(03)00122-3","article-title":"Phosphorylation of the AMPA Receptor GluR1 Subunit Is Required for Synaptic Plasticity and Retention of Spatial Memory","volume":"112","author":"Lee","year":"2003","journal-title":"Cell"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5267","DOI":"10.1016\/S0021-9258(19)34116-X","article-title":"Inhibition of Forskolin-Induced Neurite Outgrowth and Protein Phosphorylation by a Newly Synthesized Selective Inhibitor of Cyclic AMP-Dependent Protein Kinase, N-[2-(p-Bromocinnamylamino)Ethyl]-5-Isoquinolinesulfonamide (H-89), of PC12D Pheochromocytoma","volume":"265","author":"Chijiwa","year":"1990","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"15771","DOI":"10.1016\/S0021-9258(18)98476-0","article-title":"The Bisindolylmaleimide GF 109203X Is a Potent and Selective Inhibitor of Protein Kinase C","volume":"266","author":"Toullec","year":"1991","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1038\/nn1178","article-title":"LTP Is Accompanied by an Enhanced Local Excitability of Pyramidal Neuron Dendrites","volume":"7","author":"Frick","year":"2004","journal-title":"Nat. Neurosci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1113\/jphysiol.2008.158816","article-title":"Kinase-Dependent Modification of Dendritic Excitability after Long-Term Potentiation","volume":"587","author":"Rosenkranz","year":"2009","journal-title":"J. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"4534","DOI":"10.1523\/JNEUROSCI.3813-13.2014","article-title":"Dendritic Inhibition Provided by Interneuron-Specific Cells Controls the Firing Rate and Timing of the Hippocampal Feedback Inhibitory Circuitry","volume":"34","author":"Tyan","year":"2014","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3667","DOI":"10.1093\/cercor\/bhz334","article-title":"Synaptic Mechanisms Underlying the Network State-Dependent Recruitment of VIP-Expressing Interneurons in the CA1 Hippocampus","volume":"30","author":"Luo","year":"2020","journal-title":"Cereb. Cortex"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/0006-8993(92)90562-N","article-title":"Learning Impairment Following Intracerebral Administration of the HIV Envelope Protein Gp120 or a VIP Antagonist","volume":"570","author":"Glowa","year":"1992","journal-title":"Brain Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.expneurol.2007.04.004","article-title":"Vasoactive Intestinal Peptide Antagonist Treatment during Mouse Embryogenesis Impairs Social Behavior and Cognitive Function of Adult Male Offspring","volume":"206","author":"Hill","year":"2007","journal-title":"Exp. Neurol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4269","DOI":"10.1046\/j.1460-9568.1999.00865.x","article-title":"Activity-Dependent Neurotransmitter Release Kinetics: Correlation with Changes in Morphological Distributions of Small and Large Vesicles in Central Nerve Terminals","volume":"11","author":"Leenders","year":"1999","journal-title":"Eur. J. Neurosci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1002\/ddr.1132","article-title":"Adenosine Receptor Interactions in the Hippocampus","volume":"52","author":"Ribeiro","year":"2001","journal-title":"Drug Dev. Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"105356","DOI":"10.1016\/j.phrs.2020.105356","article-title":"VIPergic Neuroprotection in Epileptogenesis: Challenges and Opportunities","volume":"164","year":"2021","journal-title":"Pharmacol. Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"136268","DOI":"10.1016\/j.neulet.2021.136268","article-title":"Vasoactive Intestinal Peptide (VIP) Conducts the Neuronal Activity during Absence Seizures: GABA Seems to Be the Main Mediator of VIP","volume":"765","author":"Korkmaz","year":"2021","journal-title":"Neurosci. Lett."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/0306-4522(95)00609-5","article-title":"Different Populations of Vasoactive Intestinal Polypeptide-Immunoreactive Interneurons Are Specialized to Control Pyramidal Cells or Interneurons in the Hippocampus","volume":"73","author":"Freund","year":"1996","journal-title":"Neuroscience"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"221","DOI":"10.3389\/fncel.2020.00221","article-title":"Protective Effects of Pituitary Adenylate Cyclase-Activating Polypeptide and Vasoactive Intestinal Peptide Against Cognitive Decline in Neurodegenerative Diseases","volume":"14","author":"Vaudry","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1007\/s12031-016-0757-0","article-title":"Modulation of Corpus Striatal Neurochemistry by Astrocytes and Vasoactive Intestinal Peptide (VIP) in Parkinsonian Rats","volume":"59","author":"Yelkenli","year":"2016","journal-title":"J. Mol. Neurosci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1016\/j.peptides.2007.05.015","article-title":"Role of PACAP and VIP in Astroglial Functions","volume":"28","author":"Gandolfo","year":"2007","journal-title":"Peptides"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1007\/s12031-009-9307-3","article-title":"Vasoactive Intestinal Peptide (VIP) Treatment of Parkinsonian Rats Increases Thalamic Gamma-Aminobutyric Acid (GABA) Levels and Alters the Release of Nerve Growth Factor (NGF) by Mast Cells","volume":"41","author":"Korkmaz","year":"2010","journal-title":"J. Mol. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1038\/nature12866","article-title":"Parvalbumin-Expressing Basket-Cell Network Plasticity Induced by Experience Regulates Adult Learning","volume":"504","author":"Donato","year":"2013","journal-title":"Nature"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.brainresbull.2017.11.012","article-title":"Disinhibition in Learning and Memory Circuits: New Vistas for Somatostatin Interneurons and Long-Term Synaptic Plasticity","volume":"141","author":"Artinian","year":"2018","journal-title":"Brain Res. Bull."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.neuron.2015.07.003","article-title":"Precision of Inhibition: Dendritic Inhibition by Individual GABAergic Synapses on Hippocampal Pyramidal Cells Is Confined in Space and Time","volume":"87","author":"Wierenga","year":"2015","journal-title":"Neuron"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"5043","DOI":"10.1038\/s41467-018-07162-5","article-title":"Connectivity and Network State-Dependent Recruitment of Long-Range VIP-GABAergic Neurons in the Mouse Hippocampus","volume":"9","author":"Francavilla","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/S0306-4522(98)00455-2","article-title":"Medial Septal and Median Raphe Innervation of Vasoactive Intestinal Polypeptide-Containing Interneurons in the Hippocampus","volume":"90","author":"Papp","year":"1999","journal-title":"Neuroscience"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"8470","DOI":"10.1523\/JNEUROSCI.1413-04.2004","article-title":"Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta Activity","volume":"24","author":"Borhegyi","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"9567","DOI":"10.1523\/JNEUROSCI.2992-05.2005","article-title":"Hippocampal CA1 Circuitry Dynamically Gates Direct Cortical Inputs Preferentially at Theta Frequencies","volume":"25","author":"Ang","year":"2005","journal-title":"J. Neurosci."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/0006-8993(89)91273-0","article-title":"Activity-Induced Depression of Synaptic Inhibition during LTP-Inducing Patterned Stimulation","volume":"486","author":"Pacelli","year":"1989","journal-title":"Brain Res."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1723","DOI":"10.1016\/S0028-3908(99)00158-6","article-title":"Regulation of Depolarizing GABA(A) Receptor-Mediated Synaptic Potentials by Synaptic Activation of GABA(B) Autoreceptors in the Rat Hippocampus","volume":"38","author":"Cobb","year":"1999","journal-title":"Neuropharmacology"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"439","DOI":"10.3389\/fncel.2015.00439","article-title":"Distinct and Synergistic Feedforward Inhibition of Pyramidal Cells by Basket and Bistratified Interneurons","volume":"9","author":"Ferrante","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1460-9568.2007.06001.x","article-title":"Specific Inhibitory Synapses Shift the Balance from Feedforward to Feedback Inhibition of Hippocampal CA1 Pyramidal Cells","volume":"27","author":"Elfant","year":"2008","journal-title":"Eur. J. Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1038\/nrn1625","article-title":"Variations on an Inhibitory Theme: Phasic and Tonic Activation of GABA A Receptors","volume":"6","author":"Farrant","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.neuron.2011.12.012","article-title":"Extrasynaptic GABA A Receptors: Their Function in the CNS and Implications for Disease","volume":"73","author":"Brickley","year":"2012","journal-title":"Neuron"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"6712","DOI":"10.1073\/pnas.1507229112","article-title":"Regulation of AMPA Receptor Phosphorylation by the Neuropeptide PACAP38","volume":"112","author":"Toda","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1007\/s11064-018-2491-1","article-title":"AMPA-Type Glutamate Receptor Conductance Changes and Plasticity: Still a Lot of Noise","volume":"44","author":"Benke","year":"2019","journal-title":"Neurochem. Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.neulet.2011.03.099","article-title":"Up-Regulation of Dendritic Kv4.2 MRNA by Activation of the NMDA Receptor","volume":"496","author":"Jo","year":"2011","journal-title":"Neurosci. Lett."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1007\/s12031-018-1226-8","article-title":"Vasoactive Intestinal Peptide Decreases \u03b2-Amyloid Accumulation and Prevents Brain Atrophy in the 5xFAD Mouse Model of Alzheimer\u2019s Disease","volume":"68","author":"Korkmaz","year":"2019","journal-title":"J. Mol. Neurosci."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/5\/627\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:57:24Z","timestamp":1760137044000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/11\/5\/627"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,20]]},"references-count":66,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["biology11050627"],"URL":"https:\/\/doi.org\/10.3390\/biology11050627","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,20]]}}}