{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,8,6]],"date-time":"2025-08-06T13:15:52Z","timestamp":1754486152780,"version":"3.41.2"},"reference-count":60,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,10,14]],"date-time":"2021-10-14T00:00:00Z","timestamp":1634169600000},"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. Hum. Neurosci."],"abstract":"<jats:p>Neuroimaging, neuropsychological, and brain stimulation studies have led to contrasting findings regarding the potential roles of the lateral parietal lobe in episodic memory. Studies using brain stimulation methods reported in the literature do not offer unequivocal findings on the interactions with stimulation location (left vs. right hemisphere) or timing of the stimulation (encoding vs. retrieval). To address these issues, active and sham 1 Hz repetitive transcranial magnetic stimulation (rTMS) trains of 600 stimuli were applied over the right or left posterior parietal cortex (PPC) before the encoding or before the retrieval phase of a recognition memory task of unknown faces in a group of 40 healthy subjects. Active rTMS over the right but not the left PPC significantly improved non-verbal recognition memory performance without any significant modulation of speed of response when applied before the retrieval phase. In contrast, rTMS over the right or the left PPC before the encoding phase did not modulate memory performance. Our results support the hypothesis that the PPC plays a role in episodic memory retrieval that appears to be dependent on both the hemispheric lateralization and the timing of the stimulation (encoding vs. retrieval).<\/jats:p>","DOI":"10.3389\/fnhum.2021.696793","type":"journal-article","created":{"date-parts":[[2021,10,14]],"date-time":"2021-10-14T05:01:53Z","timestamp":1634187713000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Transcranial Magnetic Stimulation Trains at 1 Hz Frequency of the Right Posterior Parietal Cortex Facilitate Recognition Memory"],"prefix":"10.3389","volume":"15","author":[{"given":"Giuseppa Renata","family":"Mangano","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Massimiliano","family":"Oliveri","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniela","family":"Smirni","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vincenza","family":"Tarantino","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patrizia","family":"Turriziani","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2021,10,14]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"14415","DOI":"10.1523\/JNEUROSCI.4163-07.2007","article-title":"Parietal lobe and episodic memory: bilateral damage causes impaired free recall of autobiographical memory.","volume":"27","author":"Berryhill","year":"2007","journal-title":"J. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"114","DOI":"10.1016\/j.nlm.2018.12.007","article-title":"Transcranial direct current stimulation (tDCS) over parietal cortex improves associative memory.","volume":"157","author":"Bjeki\u0107","year":"2019","journal-title":"Neurobiol. Learn. Mem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"613","DOI":"10.1038\/nrn2459","article-title":"The parietal cortex and episodic memory: an attentional account.","volume":"9","author":"Cabeza","year":"2008","journal-title":"Nat. Rev.Neurosci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1097\/00019052-200008000-00008","article-title":"Neural bases of learning and memory: Functional neuroimaging evidence.","volume":"13","author":"Cabeza","year":"2000","journal-title":"Curr. Opin. Neurol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1002\/cne.902870402","article-title":"Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory cortico cortical connections.","volume":"287","author":"Cavada","year":"","journal-title":"J. Comp.Neurol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1002\/cne.902870403","article-title":"Posterior parietal cortex in rhesus monkey: II. evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe.","volume":"287","author":"Cavada","year":"","journal-title":"J. Comp.Neurol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"563768","DOI":"10.3389\/fnins.2020.563768","article-title":"Functional Interplay between posterior parietal cortex and hippocampus during detection of memory targets and non-targets.","volume":"14","author":"Ciaramelli","year":"2020","journal-title":"Front. Neurosci."},{"key":"B8","doi-asserted-by":"publisher","first-page":"1828","DOI":"10.1016\/j.neuropsychologia.2008.03.022","article-title":"Top-down and bottom-up attention to memory: a hypothesis (AtoM) on the role of the posterior parietal cortex in memory retrieval.","volume":"46","author":"Ciaramelli","year":"2008","journal-title":"Neuropsychologia"},{"key":"B9","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1016\/S0022-5371(72)80001-X","article-title":"Levels of processing. A framework for memory research.","volume":"11","author":"Craik","year":"1972","journal-title":"J. Verb. Learn. Verb. Behav."},{"key":"B10","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1162\/jocn.2009.21242","article-title":"Remember the source: dissociating frontal and parietal contributions to episodic memory.","volume":"22","author":"Donaldson","year":"2010","journal-title":"J. Cogn. Neurosci."},{"key":"B11","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1037\/a0018902","article-title":"True memory, false memory, and subjective recollection deficits after focal parietal lobe lesions.","volume":"24","author":"Drowos","year":"2010","journal-title":"Neuropsychology"},{"key":"B12","doi-asserted-by":"publisher","first-page":"175","DOI":"10.3758\/bf03193146","article-title":"G\u2217Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences.","volume":"39","author":"Faul","year":"2007","journal-title":"Behav. Res. Methods."},{"key":"B13","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1016\/j.brainres.2010.04.041","article-title":"Paired-pulse transcranial magnetic stimulation over the dorsolateral prefrontal cortex interferes with episodic encoding and retrieval for both verbal and non-verbal materials.","volume":"1344","author":"Gagnon","year":"2010","journal-title":"Brain Res."},{"key":"B14","doi-asserted-by":"publisher","first-page":"61","DOI":"10.3389\/fpsyt.2014.00061","article-title":"What makes deeply encoded items memorable? Insights into the levels of processing framework from neuroimaging and neuromodulation.","volume":"5","author":"Galli","year":"2014","journal-title":"Front. Psychiatry"},{"key":"B15","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1002\/hipo.23054","article-title":"Frequency-specific non invasive modulation of memory retrieval and its relationship with hippocampal network connectivity.","volume":"29","author":"Hermiller","year":"2019","journal-title":"Hippocampus"},{"key":"B16","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1093\/cercor\/bhs278","article-title":"Functional heterogeneity in posterior parietal cortex across attention and episodic memory retrieval.","volume":"24","author":"Hutchinson","year":"2014","journal-title":"Cereb. Cortex"},{"key":"B17","doi-asserted-by":"publisher","first-page":"129","DOI":"10.1152\/jn.00077.2008","article-title":"Distinct cortical anatomy linked to subregions of the medialtemporal lobe revealed by intrinsic functional connectivity.","volume":"100","author":"Kahn","year":"2008","journal-title":"J. Neurophysiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.nlm.2016.04.001","article-title":"A network approach for modulating memory processes via direct and indirect brain stimulation: toward a causal approach for the neural basis of memory.","volume":"134","author":"Kim","year":"2016","journal-title":"Neurobiol. Learn. Mem."},{"key":"B19","doi-asserted-by":"publisher","first-page":"eaar2768","DOI":"10.1126\/sciadv.aar2768","article-title":"Selective and coherent activity increases due to stimulation indicate functional distinctions between episodic memory networks.","volume":"4","author":"Kim","year":"2018","journal-title":"Sci. Adv."},{"key":"B20","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1080\/17588928.2018.1484723","article-title":"Transcranial magnetic stimulation of the left angular gyrus during encoding does not impair associative memory performance.","volume":"9","author":"Koen","year":"2018","journal-title":"Cogn. Neurosci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1007\/s10548-009-0126-1","article-title":"The neural bases of word encoding and retrieval: a fMRI-guided transcranial magnetic stimulation study.","volume":"22","author":"Manenti","year":"2010","journal-title":"Brain Topogr."},{"key":"B22","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1016\/j.neuropsychologia.2015.03.002","article-title":"Repetitive transcranial magnetic stimulation over the left parietal cortex facilitates visual search for a letter among its mirror images.","volume":"70","author":"Mangano","year":"2015","journal-title":"Neuropsychologia"},{"key":"B23","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1037\/0033-295X.102.3.419","article-title":"Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.","volume":"102","author":"McClelland","year":"1995","journal-title":"Psychol. Rev."},{"key":"B24","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1016\/0006-8993(77)90066-x","article-title":"Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry.","volume":"136","author":"Mesulam","year":"1977","journal-title":"Brain Res."},{"key":"B25","doi-asserted-by":"publisher","first-page":"352","DOI":"10.1002\/1098-1063200010:4<352::AID-HIPO2>3.0.CO;2-D","article-title":"Multiple trace theory of human memory: computational, neuroimaging, and neuropsychological results.","volume":"10","author":"Nadel","year":"2000","journal-title":"Hippocampus"},{"key":"B26","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1016\/j.cub.2016.12.042","article-title":"Stimulation of the posterior cortical-hippocampal network enhances precision of memory recollection.","volume":"27","author":"Nilakantan","year":"2017","journal-title":"Curr. Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"2924","DOI":"10.1523\/JNEUROSCI.4225-09.2010","article-title":"The inferior parietal lobule and recognition memory: expectancy violation or successful retrieval?","volume":"30","author":"O\u2019Connor","year":"2010","journal-title":"J. Neurosci."},{"key":"B28","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1097\/00004691-199807000-00005","article-title":"Study and modulation of human cortical excitability with transcranial magnetic stimulation.","volume":"15","author":"Pascual-Leone","year":"1998","journal-title":"J. Clin. Neurophysiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"e0123085","DOI":"10.1371\/journal.pone.0123085","article-title":"Separating recognition processes of declarative memory via anodal tDCS: boosting old item recognition by temporal and new item detection by parietal stimulation.","volume":"10","author":"Pisoni","year":"2015","journal-title":"PLoS One"},{"key":"B30","doi-asserted-by":"publisher","first-page":"948","DOI":"10.1038\/nn0901-948","article-title":"Prefrontal [correction of Prefontal] cortex in long-term memory: an \u201cinterference\u201d approach using magnetic stimulation.","volume":"4","author":"Rossi","year":"2001","journal-title":"Nat. Neurosci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"1686","DOI":"10.1016\/j.clinph.2010.12.037","article-title":"Screening questionnaire before TMS: an update.","volume":"122","author":"Rossi","year":"2011","journal-title":"Clin. Neurophysiol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1111\/j.1460-9568.2006.04600.x","article-title":"Prefrontal and parietal cortex in human episodic memory: an interference study by repetitive transcranial magnetic stimulation.","volume":"23","author":"Rossi","year":"2006","journal-title":"Eur. J. Neurosci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1016\/0013-4694(94)90029-9","article-title":"Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee.","volume":"91","author":"Rossini","year":"1994","journal-title":"Electroencephalogr. Clin. Neurophysiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1097","DOI":"10.1098\/rstb.2002.1102","article-title":"The neural basis of episodic memory: evidence from functional neuroimaging.","volume":"357","author":"Rugg","year":"2002","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"B35","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1162\/089892903322370771","article-title":"The role of prefrontal cortex in verbal episodic memory: rTMS evidence.","volume":"15","author":"Sandrini","year":"2003","journal-title":"J. Cogn. Neurosci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"066032","DOI":"10.1088\/1741-2552\/ab41ba","article-title":"Electric field simulations for transcranial brain stimulation using FEM: an efficient implementation and error analysis.","volume":"16","author":"Saturnino","year":"2019","journal-title":"J. Neural. Eng."},{"key":"B37","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1016\/j.neuropsychologia.2013.01.023","article-title":"Interference with episodic memory retrieval following transcranial stimulation of the inferior but not the superior parietal lobule.","volume":"51","author":"Sestieri","year":"2013","journal-title":"Neuropsychologia"},{"key":"B38","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1038\/nrn.2017.6","article-title":"The contribution of the human posterior parietal cortex to episodic memory.","volume":"18","author":"Sestieri","year":"2017","journal-title":"Nat. Rev. Neurosci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"277","DOI":"10.3758\/s13415-011-0031-4","article-title":"Episodic retrieval and the cortical binding of relational activity.","volume":"11","author":"Shimamura","year":"2011","journal-title":"Cogn. Affect. Behav. Neurosci."},{"key":"B40","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1093\/cercor\/bhp116","article-title":"Dissociation between memory accuracy and memory confidence following bilateral parietal lesions.","volume":"20","author":"Simons","year":"2010","journal-title":"Cereb. Cortex"},{"key":"B41","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1038\/nrn1178","article-title":"Prefrontal and medial temporal lobe interactions in long-term memory.","volume":"4","author":"Simons","year":"2003","journal-title":"Nat. Rev. Neurosci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1391","DOI":"10.1007\/s10072-018-3433-z","article-title":"Standardization and validation of a parallel form of the verbal and non-verbal recognition memory test in an Italian population sample.","volume":"39","author":"Smirni","year":"2018","journal-title":"Neurol. Sci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"e0144838","DOI":"10.1371\/journal.pone.0144838","article-title":"Modulating memory performance in healthy subjects with transcranial direct current stimulation over the right dorsolateral prefrontal cortex.","volume":"10","author":"Smirni","year":"2015","journal-title":"PLoS One"},{"key":"B44","first-page":"227","article-title":"Standardizzazione di tre nuovi test di memoria di riconoscimento verbale e non verbale: uno studio preliminare.","volume":"1","author":"Smirni","year":"2010","journal-title":"G. Ital. Psicol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"137","DOI":"10.3758\/bf03207704","article-title":"Calculation of signal detection theory measures.","volume":"31","author":"Stanislaw","year":"1999","journal-title":"Behav. Res. Methods Instrum. Comput."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1452","DOI":"10.1162\/jocn_a_01300","article-title":"Hippocampal-targeted theta-burst stimulation enhances associative memory formation.","volume":"30","author":"Tambini","year":"2018","journal-title":"J. Cogn. Neurosci."},{"key":"B47","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1037\/\/0735-7044.100.2.147","article-title":"The hippocampal memory indexing theory.","volume":"100","author":"Teyler","year":"1986","journal-title":"Behav. Neurosci."},{"key":"B48","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1007\/s00221-007-0991-3","article-title":"Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models.","volume":"180","author":"Thickbroom","year":"2007","journal-title":"Exp. Brain Res."},{"key":"B49","doi-asserted-by":"publisher","first-page":"613","DOI":"10.3233\/JAD-190888","article-title":"Low-frequency repetitive transcranial magnetic stimulation of the right dorsolateral prefrontal cortex enhances recognition memory in Alzheimer\u2019s disease.","volume":"72","author":"Turriziani","year":"2019","journal-title":"J. Alzheimers Dis."},{"key":"B50","doi-asserted-by":"publisher","first-page":"62","DOI":"10.3389\/fnhum.2012.00062","article-title":"Enhancing memory performance with rTMS in healthy subjects and individuals with mild cognitive impairment: the role of the right dorsolateral prefrontal cortex.","volume":"10","author":"Turriziani","year":"2012","journal-title":"Front. Hum. Neurosci."},{"key":"B51","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1016\/j.nlm.2008.10.011","article-title":"Posterior parietal cortex and episodic encoding: insights from fMRI subsequent memory effects and dual attention theory.","volume":"91","author":"Uncapher","year":"2009","journal-title":"Neurobiol. Learn. Mem."},{"key":"B52","doi-asserted-by":"publisher","first-page":"1787","DOI":"10.1016\/j.neuropsychologia.2008.01.004","article-title":"Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective.","volume":"46","author":"Vilberg","year":"2008","journal-title":"Neuropsychologia"},{"key":"B53","doi-asserted-by":"publisher","first-page":"3328","DOI":"10.1152\/jn.90355.2008","article-title":"Evidence for a frontoparietal control system revealed by intrinsic functional connectivity.","volume":"100","author":"Vincent","year":"2008","journal-title":"J. Neurophysiol."},{"key":"B54","doi-asserted-by":"publisher","first-page":"3517","DOI":"10.1152\/jn.00048.2006","article-title":"Coherent spontaneous activity identifies a hippocampal-parietal memory network.","volume":"96","author":"Vincent","year":"2006","journal-title":"J. Neurophysiol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"3013","DOI":"10.1038\/s41598-021-82577-7","article-title":"Theta-modulated oscillatory transcranial direct current stimulation over posterior parietal cortex improves associative memory.","volume":"11","author":"Vuli\u0107","year":"2021","journal-title":"Sci. Rep."},{"key":"B56","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1016\/j.tics.2005.07.001","article-title":"Parietal lobe contributions to episodic memory retrieval.","volume":"9","author":"Wagner","year":"2005","journal-title":"Trends Cogn. Sci."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1054","DOI":"10.1126\/science.1252900","article-title":"Memory enhancement: targeted enhancement of cortical-hippocampal brain networks and associative memory.","volume":"345","author":"Wang","year":"2014","journal-title":"Science"},{"key":"B58","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1038\/nn.3315","article-title":"Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval.","volume":"16","author":"Watrous","year":"2013","journal-title":"Nat. Neurosci."},{"key":"B59","doi-asserted-by":"publisher","first-page":"766","DOI":"10.1017\/S1355617711000683","article-title":"Memory transformation and systems consolidation.","volume":"17","author":"Winocur","year":"2011","journal-title":"J. Int. Neuropsychol. Soc."},{"key":"B60","doi-asserted-by":"publisher","first-page":"993","DOI":"10.3389\/fpsyg.2019.00993","article-title":"How can transcranial magnetic stimulation be used to modulate episodic memory: a systematic review and meta-analysis.","volume":"10","author":"Yeh","year":"2019","journal-title":"Front. Psychol."}],"container-title":["Frontiers in Human Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnhum.2021.696793\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,14]],"date-time":"2021-10-14T05:01:58Z","timestamp":1634187718000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnhum.2021.696793\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,14]]},"references-count":60,"alternative-id":["10.3389\/fnhum.2021.696793"],"URL":"https:\/\/doi.org\/10.3389\/fnhum.2021.696793","relation":{},"ISSN":["1662-5161"],"issn-type":[{"type":"electronic","value":"1662-5161"}],"subject":[],"published":{"date-parts":[[2021,10,14]]},"article-number":"696793"}}