{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T04:20:31Z","timestamp":1787026831762,"version":"build-2736575974"},"reference-count":58,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,2,28]],"date-time":"2025-02-28T00:00:00Z","timestamp":1740700800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neural Circuits"],"abstract":"<jats:p>Experience-dependent neural plasticity enables the brain to adapt to diverse and dynamic environments by reshaping circuits. In the adult visual system, this plasticity can be elicited by repeated sensory stimuli; however, its temporal dynamics and underlying mechanisms remain unclear. Here, we investigated the regulation of visual response potentiation induced by repeated light flashes in the primary visual cortex of awake adult mice. Our findings revealed two distinct temporal phases of potentiation: a rapid phase occurring within seconds and a cumulative phase developing over hours to days. Notably, the identification of this rapid phase phenomenon adds to and refines the prevailing view that visual plasticity in the adult cortex is predominantly slow. Additionally, exposure to visual stimuli enhanced spontaneous slow-wave activity in the visual cortex during non-REM sleep. This plasticity was significantly impaired in Grin2a (NR2A) knockout mice, a model of schizophrenia, which mirrors visual plasticity deficits observed in human patients. The dual temporal characteristics of flash-evoked visual plasticity likely reflect multifaceted aspects of adult brain functionality, encompassing processes related to memory, learning, and neurological disorders. This model of visual plasticity in defined neural circuits provides a simplified yet robust and extensible framework for exploring the neural mechanisms underlying adaptive and maladaptive behavioral changes.<\/jats:p>","DOI":"10.3389\/fncir.2025.1537305","type":"journal-article","created":{"date-parts":[[2025,2,28]],"date-time":"2025-02-28T02:08:10Z","timestamp":1740708490000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Rapid and cumulative adult plasticity in the mouse visual cortex"],"prefix":"10.3389","volume":"19","author":[{"given":"Hiroyuki","family":"Miyamoto","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emi","family":"Mazaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuichi","family":"Makino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi","family":"Fang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomohito","family":"Hamada","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youichi","family":"Handa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takao K.","family":"Hensch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,2,28]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"758","DOI":"10.1038\/nn1072","article-title":"Early 'visual' cortex activation correlates with superior verbal memory performance in the blind","volume":"6","author":"Amedi","year":"2003","journal-title":"Nat. Neurosci."},{"key":"ref2","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":"ref3","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1016\/j.cub.2011.03.065","article-title":"Improvement and impairment of visually guided behavior through LTP- and LTD-like exposure-based visual learning","volume":"21","author":"Beste","year":"2011","journal-title":"Curr. Biol."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"512","DOI":"10.1016\/j.biopsych.2012.01.013","article-title":"Impaired visual cortical plasticity in schizophrenia","volume":"71","author":"Cavus","year":"2012","journal-title":"Biol. Psychiatry"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"84630","DOI":"10.7554\/eLife.84630.3","article-title":"Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice","volume":"12","author":"Claar","year":"2023","journal-title":"eLife"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1016\/j.biopsych.2011.08.021","article-title":"Translating long-term potentiation from animals to humans: a novel method for noninvasive assessment of cortical plasticity","volume":"71","author":"Clapp","year":"2012","journal-title":"Biol. Psychiatry"},{"key":"ref7","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":"ref8","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1038\/nature03275","article-title":"How sleep affects the developmental learning of bird song","volume":"433","author":"Deregnaucourt","year":"2005","journal-title":"Nature"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"155","DOI":"10.5665\/sleep.5338","article-title":"Sleep-dependent potentiation in the visual system is at odds with the synaptic homeostasis hypothesis","volume":"39","author":"Durkin","year":"2016","journal-title":"Sleep"},{"key":"ref10","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":"ref11","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. USA"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/0031-9384(89)90140-6","article-title":"Peak N160 of rat flash evoked potential: does it reflect habituation or sensitization?","volume":"45","author":"Dyer","year":"1989","journal-title":"Physiol. Behav."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.brainresbull.2021.01.019","article-title":"Reduced visual cortical plasticity in autism spectrum disorder","volume":"170","author":"Ellis","year":"2021","journal-title":"Brain Res. Bull."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"2854","DOI":"10.1073\/pnas.0536089100","article-title":"Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling","volume":"100","author":"Fagiolini","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1152\/physrev.00042.2018","article-title":"Sleep spindles: mechanisms and functions","volume":"100","author":"Fernandez","year":"2020","journal-title":"Physiol. Rev."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"39111","DOI":"10.7554\/eLife.39111","article-title":"Thalamic reticular control of local sleep in mouse sensory cortex","volume":"7","author":"Fernandez","year":"2018","journal-title":"eLife"},{"key":"ref17","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":"ref18","doi-asserted-by":"publisher","first-page":"732","DOI":"10.1038\/nn.3683","article-title":"Learned spatiotemporal sequence recognition and prediction in primary visual cortex","volume":"17","author":"Gavornik","year":"2014","journal-title":"Nat. Neurosci."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"e0184618","DOI":"10.1371\/journal.pone.0184618","article-title":"Rapid plasticity of visually evoked responses in rat monocular visual cortex","volume":"12","author":"Griffen","year":"2017","journal-title":"PLoS One"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"7307","DOI":"10.1523\/JNEUROSCI.0090-23.2023","article-title":"Electrophysiological signatures of visual recognition memory across all layers of mouse V1","volume":"43","author":"Hayden","year":"2023","journal-title":"J. Neurosci."},{"key":"ref21","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":"ref22","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1038\/nrn1787","article-title":"Critical period plasticity in local cortical circuits","volume":"6","author":"Hensch","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"E014","DOI":"10.1017\/S0952523817000219","article-title":"Critical periods in amblyopia","volume":"35","author":"Hensch","year":"2018","journal-title":"Vis. Neurosci."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/0031-9384(91)90056-T","article-title":"Rat flash-evoked potential peak N160 amplitude: modulation by relative flash intensity","volume":"49","author":"Herr","year":"1991","journal-title":"Physiol. Behav."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1016\/0031-9384(94)90014-0","article-title":"Within-session changes in peak N160 amplitude of flash evoked potentials in rats","volume":"55","author":"Herr","year":"1994","journal-title":"Physiol. Behav."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1038\/s41398-023-02393-7","article-title":"Mouse mutants in schizophrenia risk genes GRIN2A and AKAP11 show EEG abnormalities in common with schizophrenia patients","volume":"13","author":"Herzog","year":"2023","journal-title":"Transl. Psychiatry"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"9801","DOI":"10.1523\/JNEUROSCI.21-24-09801.2001","article-title":"Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo","volume":"21","author":"Heynen","year":"2001","journal-title":"J. Neurosci."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"1671","DOI":"10.1152\/jn.00915.2004","article-title":"Modeling sleep and wakefulness in the thalamocortical system","volume":"93","author":"Hill","year":"2005","journal-title":"J. Neurophysiol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1038\/nature02663","article-title":"Local sleep and learning","volume":"430","author":"Huber","year":"2004","journal-title":"Nature"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"3532","DOI":"10.1523\/JNEUROSCI.3760-16.2017","article-title":"Locomotion induces stimulus-specific response enhancement in adult visual cortex","volume":"37","author":"Kaneko","year":"2017","journal-title":"J. Neurosci."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"11450","DOI":"10.7554\/eLife.11450","article-title":"Contrasting roles for parvalbumin-expressing inhibitory neurons in two forms of adult visual cortical plasticity","volume":"5","author":"Kaplan","year":"2016","journal-title":"eLife"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"555","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":"ref33","doi-asserted-by":"publisher","first-page":"tgab016","DOI":"10.1093\/texcom\/tgab016","article-title":"High-frequency visual stimulation primes gamma oscillations for visually evoked phase reset and enhances spatial acuity","volume":"2","author":"Lantz","year":"2021","journal-title":"Cereb Cortex Commun."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1146\/annurev-neuro-090919-022842","article-title":"Synaptic plasticity forms and functions","volume":"43","author":"Magee","year":"2020","journal-title":"Annu. Rev. Neurosci."},{"key":"ref35","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":"ref36","doi-asserted-by":"publisher","first-page":"3835","DOI":"10.1016\/j.celrep.2019.11.075","article-title":"Physiological signature of memory age in the prefrontal-hippocampal circuit","volume":"29","author":"Makino","year":"2019","journal-title":"Cell Rep."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1038\/nn1064","article-title":"Experience-dependent slow-wave sleep development","volume":"6","author":"Miyamoto","year":"2003","journal-title":"Nat. Neurosci."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1917","DOI":"10.1038\/s41467-019-09954-9","article-title":"Impaired cortico-striatal excitatory transmission triggers epilepsy","volume":"10","author":"Miyamoto","year":"2019","journal-title":"Nat. Commun."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"815554","DOI":"10.3389\/fncir.2021.815554","article-title":"Stimulus-selective response plasticity in primary visual cortex: Progress and puzzles","volume":"15","author":"Montgomery","year":"2022","journal-title":"Front. Neural. Circuits"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"578","DOI":"10.1038\/s41586-022-05045-w","article-title":"Modular strategy for development of the hierarchical visual network in mice","volume":"608","author":"Murakami","year":"2022","journal-title":"Nature"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1016\/j.neuron.2015.07.033","article-title":"Excitatory\/inhibitory balance and circuit homeostasis in autism Spectrum disorders","volume":"87","author":"Nelson","year":"2015","journal-title":"Neuron"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1016\/j.biopsych.2006.10.006","article-title":"Long-term plasticity of visually evoked potentials in humans is altered in major depression","volume":"62","author":"Normann","year":"2007","journal-title":"Biol. Psychiatry"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"8958","DOI":"10.1523\/JNEUROSCI.1151-11.2011","article-title":"Role of cerebellar cortical protein synthesis in transfer of memory trace of cerebellum-dependent motor learning","volume":"31","author":"Okamoto","year":"2011","journal-title":"J. Neurosci."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1016\/j.schres.2018.08.025","article-title":"Synaptic plasticity\/dysplasticity, process memory and item memory in rodent models of mental dysfunction","volume":"207","author":"O'Reilly","year":"2019","journal-title":"Schizophr. Res."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"2833","DOI":"10.1016\/S0042-6989(99)00016-4","article-title":"Properties of the flash visual evoked potential recorded in the cat primary visual cortex","volume":"39","author":"Padnick","year":"1999","journal-title":"Vis. Res."},{"key":"ref46","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1038\/s42003-022-03012-9","article-title":"Plasticity in visual cortex is disrupted in a mouse model of tauopathy","volume":"5","author":"Papanikolaou","year":"2022","journal-title":"Commun. Biol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"3071","DOI":"10.1016\/S0042-6989(99)00022-X","article-title":"The visual physiology of the wild type mouse determined with pattern VEPs","volume":"39","author":"Porciatti","year":"1999","journal-title":"Vis. Res."},{"key":"ref48","doi-asserted-by":"publisher","first-page":"12876","DOI":"10.1073\/pnas.96.22.12876","article-title":"Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development","volume":"96","author":"Quinlan","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1038\/373151a0","article-title":"Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor epsilon 1 subunit","volume":"373","author":"Sakimura","year":"1995","journal-title":"Nature"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1093\/cercor\/8.7.575","article-title":"A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque","volume":"8","author":"Schroeder","year":"1998","journal-title":"Cereb. Cortex"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1016\/j.neuron.2018.12.009","article-title":"Layer-specific physiological features and interlaminar interactions in the primary visual cortex of the mouse","volume":"101","author":"Senzai","year":"2019","journal-title":"Neuron"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"108152","DOI":"10.1016\/j.celrep.2020.108152","article-title":"Visual sequences drive experience-dependent plasticity in mouse anterior cingulate cortex","volume":"32","author":"Sidorov","year":"2020","journal-title":"Cell Rep."},{"key":"ref53","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1038\/s41586-022-04556-w","article-title":"Rare coding variants in ten genes confer substantial risk for schizophrenia","volume":"604","author":"Singh","year":"2022","journal-title":"Nature"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.neuron.2013.07.022","article-title":"A theory of the transition to critical period plasticity: inhibition selectively suppresses spontaneous activity","volume":"80","author":"Toyoizumi","year":"2013","journal-title":"Neuron"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"3925","DOI":"10.1152\/jn.00724.2005","article-title":"Photic-induced sensitization: acquisition of an augmenting spike-wave response in the adult rat through repeated strobe exposure","volume":"94","author":"Uhlrich","year":"2005","journal-title":"J. Neurophysiol."},{"key":"ref56","doi-asserted-by":"publisher","first-page":"1751","DOI":"10.1093\/schbul\/sbab049","article-title":"Evidence for reduced long-term potentiation-like visual cortical plasticity in schizophrenia and bipolar disorder","volume":"47","author":"Valstad","year":"2021","journal-title":"Schizophr. Bull."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1046\/j.1365-2869.2000.00230.x","article-title":"Unilateral vibrissae stimulation during waking induces interhemispheric EEG asymmetry during subsequent sleep in the rat","volume":"9","author":"Vyazovskiy","year":"2000","journal-title":"J. Sleep Res."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1002\/cne.21286","article-title":"Area map of mouse visual cortex","volume":"502","author":"Wang","year":"2007","journal-title":"J. Comp. Neurol."}],"container-title":["Frontiers in Neural Circuits"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncir.2025.1537305\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,28]],"date-time":"2025-02-28T02:08:16Z","timestamp":1740708496000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncir.2025.1537305\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,28]]},"references-count":58,"alternative-id":["10.3389\/fncir.2025.1537305"],"URL":"https:\/\/doi.org\/10.3389\/fncir.2025.1537305","relation":{},"ISSN":["1662-5110"],"issn-type":[{"value":"1662-5110","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,2,28]]},"article-number":"1537305"}}