{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,19]],"date-time":"2026-08-19T19:02:20Z","timestamp":1787166140277,"version":"build-2736575974"},"reference-count":49,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T00:00:00Z","timestamp":1649376000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000268","name":"Biotechnology and Biological Sciences Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000268","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Neurosci."],"abstract":"<jats:p>Recognizing familiar but innocuous stimuli and suppressing behavioral response to those stimuli are critical steps in dedicating cognitive resources to significant elements of the environment. Recent work in the visual system has uncovered key neocortical mechanisms of this familiarity that emerges over days. Specifically, exposure to phase-reversing gratings of a specific orientation causes long-lasting stimulus-selective response potentiation (SRP) in layer 4 of mouse primary visual cortex (V1) as the animal\u2019s behavioral responses are reduced through habituation. This plasticity and concomitant learning require the NMDA receptor and the activity of parvalbumin-expressing (PV+) inhibitory neurons. Changes over the course of seconds and minutes have been less well studied in this paradigm, so we have here characterized cortical plasticity occurring over seconds and minutes, as well as days, to identify separable forms of plasticity accompanying familiarity. In addition, we show evidence of interactions between plasticity over these different timescales and reveal key mechanistic differences. Layer 4 visual-evoked potentials (VEPs) are potentiated over days, and they are depressed over minutes, even though both forms of plasticity coincide with significant reductions in behavioral response. Adaptation, classically described as a progressive reduction in synaptic or neural activity, also occurs over the course of seconds, but appears mechanistically separable over a second as compared to tens of seconds. Interestingly, these short-term forms of adaptation are modulated by long-term familiarity, such that they occur for novel but not highly familiar stimuli. Genetic knock-down of NMDA receptors within V1 prevents all forms of plasticity while, importantly, the modulation of short-term adaptation by long-term familiarity is gated by PV+ interneurons. Our findings demonstrate that different timescales of adaptation\/habituation have divergent but overlapping mechanisms, providing new insight into how the brain is modified by experience to encode familiarity.<\/jats:p>","DOI":"10.3389\/fncel.2022.840057","type":"journal-article","created":{"date-parts":[[2022,4,8]],"date-time":"2022-04-08T16:49:27Z","timestamp":1649436567000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":6,"title":["Multiple Mechanistically Distinct Timescales of Neocortical Plasticity Occur During Habituation"],"prefix":"10.3389","volume":"16","author":[{"given":"Francesca A.","family":"Chaloner","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sam F.","family":"Cooke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,4,8]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/j.neuron.2011.12.013","article-title":"Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli.","volume":"73","author":"Atallah","year":"2012","journal-title":"Neuron"},{"key":"B2","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.5665\/sleep.3830","article-title":"Sleep promotes cortical response potentiation following visual experience.","volume":"37","author":"Aton","year":"2014","journal-title":"Sleep"},{"key":"B3","doi-asserted-by":"publisher","first-page":"2987","DOI":"10.1152\/jn.00283.2003","article-title":"Two dynamically distinct inhibitory networks in layer 4 of the neocortex.","volume":"90","author":"Beierlein","year":"2003","journal-title":"J. Neurophysiol."},{"key":"B4","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1038\/361031a0","article-title":"A synaptic model of memory: long-term potentiation in the hippocampus.","volume":"361","author":"Bliss","year":"1993","journal-title":"Nature"},{"key":"B5","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1038\/nrn3241","article-title":"The origin of extracellular fields and currents\u2013EEG, ECoG, LFP and spikes.","volume":"13","author":"Buzs\u00e1ki","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"12560","DOI":"10.1523\/JNEUROSCI.2240-15.2015","article-title":"Specific Early and Late Oddball-Evoked Responses in Excitatory and Inhibitory Neurons of Mouse Auditory Cortex.","volume":"35","author":"Chen","year":"2015","journal-title":"J. Neurosci."},{"key":"B7","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/s0896-6273(02)00659-1","article-title":"Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo.","volume":"34","author":"Chung","year":"2002","journal-title":"Neuron"},{"key":"B8","doi-asserted-by":"publisher","first-page":"16304","DOI":"10.1523\/JNEUROSCI.4333-10.2010","article-title":"Visual experience induces long-term potentiation in the primary visual cortex.","volume":"30","author":"Cooke","year":"2010","journal-title":"J. Neurosci."},{"key":"B9","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1038\/nn.3920","article-title":"Visual recognition memory, manifested as long-term habituation, requires synaptic plasticity in V1.","volume":"18","author":"Cooke","year":"2015","journal-title":"Nat. Neurosci."},{"key":"B10","doi-asserted-by":"crossref","first-page":"197","DOI":"10.7551\/mitpress\/11442.003.0025","article-title":"Ignoring the Innocuous: the Neural Mechanisms of Habituation","author":"Cooke","year":"2020","journal-title":"The Cognitive Neurosciences"},{"key":"B11","doi-asserted-by":"publisher","first-page":"19567","DOI":"10.1523\/JNEUROSCI.2624-13.2013","article-title":"Target-specific effects of somatostatin-expressing interneurons on neocortical visual processing.","volume":"33","author":"Cottam","year":"2013","journal-title":"J. Neurosci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.neuron.2009.12.025","article-title":"Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons.","volume":"65","author":"Cruikshank","year":"2010","journal-title":"Neuron"},{"key":"B13","doi-asserted-by":"publisher","first-page":"4327","DOI":"10.1016\/j.cub.2021.07.062","article-title":"Representational drift in the mouse visual.","volume":"31","author":"Deitch","year":"2021","journal-title":"Curr. Biol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"10485","DOI":"10.1073\/pnas.1710613114","article-title":"Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity.","volume":"114","author":"Durkin","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B15","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1146\/annurev-vision-091718-014715","article-title":"How sleep shapes thalamocortical circuit function in the visual system.","volume":"5","author":"Durkin","year":"2019","journal-title":"Annu. Rev. Vis. Sci."},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1101\/2021.03.01.433430","article-title":"The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity.","author":"Finnie","year":"2021","journal-title":"BioRxiv"},{"key":"B17","doi-asserted-by":"publisher","first-page":"2555","DOI":"10.1093\/cercor\/bhz260","article-title":"Distinct Laminar Requirements for NMDA Receptors in Experience-Dependent Visual Cortical Plasticity.","volume":"30","author":"Fong","year":"2020","journal-title":"Cereb. Cortex"},{"key":"B18","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/j.neuron.2006.06.026","article-title":"Instructive effect of visual experience in mouse visual cortex.","volume":"51","author":"Frenkel","year":"2006","journal-title":"Neuron"},{"key":"B19","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1016\/j.clinph.2008.11.029","article-title":"The mismatch negativity: a review of underlying mechanisms.","volume":"120","author":"Garrido","year":"2009","journal-title":"Clin. Neurophysiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1037\/h0029810","article-title":"Habituation: a dual-process theory.","volume":"77","author":"Groves","year":"1970","journal-title":"Psychol. Rev."},{"key":"B21","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1016\/j.celrep.2016.06.037","article-title":"Somatostatin interneurons control a key component of mismatch negativity in mouse visual cortex.","volume":"16","author":"Hamm","year":"2016","journal-title":"Cell Rep."},{"key":"B22","doi-asserted-by":"publisher","first-page":"6257","DOI":"10.1523\/JNEUROSCI.0391-21.2021","article-title":"Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex.","volume":"41","author":"Hayden","year":"2021","journal-title":"J. Neurosci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/215707a0","article-title":"Neuronal mechanisms of habituation.","volume":"215","author":"Horn","year":"1967","journal-title":"Nature"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.11450","article-title":"Contrasting roles for parvalbumin-expressing inhibitory neurons in two forms of adult visual cortical plasticity.","author":"Kaplan","year":"2016","journal-title":"eLife"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.1016\/j.neuron.2015.10.024","article-title":"Flexible sensory representations in auditory cortex driven by behavioral relevance.","volume":"88","author":"Kato","year":"2015","journal-title":"Neuron"},{"key":"B26","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.neuron.2008.11.016","article-title":"Local origin of field potentials in visual cortex.","volume":"61","author":"Katzner","year":"2009","journal-title":"Neuron"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2019.00555","article-title":"Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex.","volume":"13","author":"Kim","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"B28","author":"Konorski","year":"1967"},{"key":"B29","doi-asserted-by":"publisher","first-page":"1151","DOI":"10.1016\/s0896-6273(00)80632-7","article-title":"NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus.","volume":"21","author":"Lee","year":"1998","journal-title":"Neuron"},{"key":"B30","doi-asserted-by":"publisher","first-page":"3429","DOI":"10.1152\/jn.00456.2003","article-title":"Two distinct types of corticothalamic EPSPs and their contribution to short-term synaptic plasticity.","volume":"90","author":"Li","year":"2003","journal-title":"J. Neurophysiol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.1038\/nn.4061","article-title":"Learning enhances the relative impact of top-down processing in the visual cortex.","volume":"18","author":"Makino","year":"2015","journal-title":"Nat. Neurosci."},{"key":"B32","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1016\/j.neubiorev.2017.05.028","article-title":"Habituation is altered in neuropsychiatric disorders-A comprehensive review with recommendations for experimental design and analysis.","volume":"80","author":"McDiarmid","year":"2017","journal-title":"Neurosci. Biobehav. Rev."},{"key":"B33","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1126\/science.287.5451.248","article-title":"Memory\u2013a century of consolidation.","volume":"287","author":"McGaugh","year":"2000","journal-title":"Science"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2021.815554","article-title":"Stimulus-Selective Response Plasticity in Primary Visual Cortex: progress and Puzzles.","volume":"15","author":"Montgomery","year":"2021","journal-title":"Front. Neural Circuits"},{"key":"B35","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1177\/1073858405282431","article-title":"Synaptic vesicles: turning reluctance into action.","volume":"12","author":"Moulder","year":"2006","journal-title":"Neuroscientist"},{"key":"B36","doi-asserted-by":"publisher","first-page":"2544","DOI":"10.1016\/j.clinph.2007.04.026","article-title":"The mismatch negativity (MMN) in basic research of central auditory processing: a review.","volume":"118","author":"N\u00e4\u00e4t\u00e4nen","year":"2007","journal-title":"Clin. Neurophysiol."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.09868","article-title":"Complementary control of sensory adaptation by two types of cortical interneurons.","volume":"4","author":"Natan","year":"2015","journal-title":"eLife"},{"key":"B38","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1038\/nrn2303","article-title":"Synaptic plasticity, memory and the hippocampus: a neural network approach to causality.","volume":"9","author":"Neves","year":"2008","journal-title":"Nat. Rev. Neurosci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1068","DOI":"10.1038\/nn.3446","article-title":"Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons.","volume":"16","author":"Pfeffer","year":"2013","journal-title":"Nat. Neurosci."},{"key":"B40","doi-asserted-by":"publisher","first-page":"2052","DOI":"10.1523\/JNEUROSCI.1459-18.2018","article-title":"Superficial layers suppress the deep layers to fine-tune cortical coding","volume":"39","author":"Pluta","year":"2019","journal-title":"J. Neurosci"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1216","DOI":"10.1016\/j.neuron.2014.04.035","article-title":"Network plasticity in adaptive filtering and behavioral habituation.","volume":"82","author":"Ramaswami","year":"2014","journal-title":"Neuron"},{"key":"B42","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1016\/j.nlm.2008.09.012","article-title":"Habituation revisited: an updated and revised description of the behavioral characteristics of habituation.","volume":"92","author":"Rankin","year":"2009","journal-title":"Neurobiol. Learn. Mem."},{"key":"B43","doi-asserted-by":"publisher","first-page":"8761","DOI":"10.1523\/JNEUROSCI.3176-20.2021","article-title":"Reliable sensory processing in mouse visual cortex through cooperative interactions between somatostatin and parvalbumin interneurons.","volume":"41","author":"Rikhye","year":"2021","journal-title":"J. Neurosci."},{"key":"B44","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1037\/a0021461","article-title":"Competitive short-term and long-term memory processes in spatial habituation.","volume":"37","author":"Sanderson","year":"2011","journal-title":"J. Exp. Psychol. Anim. Behav. Process."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.3389\/fnint.2014.00097","article-title":"Habituation mechanisms and their importance for cognitive function.","volume":"8","author":"Schmid","year":"2014","journal-title":"Front. Integr. Neurosci."},{"key":"B46","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1146\/annurev.ph.25.030163.002553","article-title":"Higher nervous functions; the orienting reflex.","volume":"25","author":"Sokolov","year":"1963","journal-title":"Annu. Rev. Physiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"13837","DOI":"10.1523\/JNEUROSCI.3475-09.2009","article-title":"Correlating stimulus-specific adaptation of cortical neurons and local field potentials in the awake rat.","volume":"29","author":"von der Behrens","year":"2009","journal-title":"J. Neurosci."},{"key":"B48","article-title":"\u201cSOP: A model of automatic memory processing in animal behavior,\u201d in","author":"Wagner","year":"1981","journal-title":"Information Processing in Animals"},{"key":"B49","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/j.neuron.2012.11.004","article-title":"Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4.","volume":"77","author":"Xu","year":"2013","journal-title":"Neuron"}],"container-title":["Frontiers in Cellular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2022.840057\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,31]],"date-time":"2023-01-31T23:59:44Z","timestamp":1675209584000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2022.840057\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,8]]},"references-count":49,"alternative-id":["10.3389\/fncel.2022.840057"],"URL":"https:\/\/doi.org\/10.3389\/fncel.2022.840057","relation":{},"ISSN":["1662-5102"],"issn-type":[{"value":"1662-5102","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,8]]},"article-number":"840057"}}