{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T05:51:57Z","timestamp":1790747517423,"version":"4.1.0"},"reference-count":82,"publisher":"Wiley","license":[{"start":{"date-parts":[[2021,1,14]],"date-time":"2021-01-14T00:00:00Z","timestamp":1610582400000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01-NS097498(MAS)"],"award-info":[{"award-number":["R01-NS097498(MAS)"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01-DC004825(SES)"],"award-info":[{"award-number":["R01-DC004825(SES)"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Neural Plasticity"],"published-print":{"date-parts":[[2021,1,14]]},"abstract":"<jats:p>Accumulating evidence implicates a role for brain structures outside the ascending auditory pathway in tinnitus, the phantom perception of sound. In addition to other factors such as age-dependent hearing loss, high-level sound exposure is a prominent cause of tinnitus. Here, we examined how noise exposure altered the distribution of excitatory and inhibitory synaptic inputs in the guinea pig hippocampus and determined whether these changes were associated with tinnitus. In experiment one, guinea pigs were overexposed to unilateral narrow-band noise (98\u2009dB SPL, 2\u2009h). Two weeks later, the density of excitatory (VGLUT-1\/2) and inhibitory (VGAT) synaptic terminals in CA1, CA3, and dentate gyrus hippocampal subregions was assessed by immunohistochemistry. Overall, VGLUT-1 density primarily increased, while VGAT density decreased significantly in many regions. Then, to assess whether the noise-induced alterations were persistent and related to tinnitus, experiment two utilized a noise-exposure paradigm shown to induce tinnitus and assessed tinnitus development which was assessed using gap-prepulse inhibition of the acoustic startle (GPIAS). Twelve weeks after sound overexposure, changes in excitatory synaptic terminal density had largely recovered regardless of tinnitus status, but the recovery of GABAergic terminal density was dramatically different in animals expressing tinnitus relative to animals resistant to tinnitus. In resistant animals, inhibitory synapse density recovered to preexposure levels, but in animals expressing tinnitus, inhibitory synapse density remained chronically diminished. Taken together, our results suggest that noise exposure induces striking changes in the balance of excitatory and inhibitory synaptic inputs throughout the hippocampus and reveal a potential role for rebounding inhibition in the hippocampus as a protective factor leading to tinnitus resilience.<\/jats:p>","DOI":"10.1155\/2021\/8833087","type":"journal-article","created":{"date-parts":[[2021,1,15]],"date-time":"2021-01-15T19:50:06Z","timestamp":1610740206000},"page":"1-16","source":"Crossref","is-referenced-by-count":23,"title":["Noise Exposure Alters Glutamatergic and GABAergic Synaptic Connectivity in the Hippocampus and Its Relevance to Tinnitus"],"prefix":"10.1155","volume":"2021","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0844-0567","authenticated-orcid":true,"given":"Liqin","family":"Zhang","sequence":"first","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Molecular & Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Department of Otolaryngology, Peking Union Medical College Hospital, Beijing, China"},{"name":"Xiangya Medical School, Central South University, Changsha, Hunan, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Calvin","family":"Wu","sequence":"additional","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0165-6429","authenticated-orcid":true,"given":"David T.","family":"Martel","sequence":"additional","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"West","sequence":"additional","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1593-727X","authenticated-orcid":true,"given":"Michael A.","family":"Sutton","sequence":"additional","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Molecular & Behavioral Neuroscience Institute, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5300-5492","authenticated-orcid":true,"given":"Susan E.","family":"Shore","sequence":"additional","affiliation":[{"name":"Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Department of Biomedical Engineering, University of Michigan, Ann Arbor, Michigan, USA"},{"name":"Department of Molecular and Integrative Physiology, University of Michigan, Ann Arbor, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","reference":[{"issue":"3","key":"1","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/j.jpsychores.2010.03.008","article-title":"The association between tinnitus and mental health in a general population sample: results from the HUNT Study","volume":"69","author":"N. H. Krog","year":"2010","journal-title":"Journal of Psychosomatic Research"},{"key":"2","doi-asserted-by":"publisher","DOI":"10.1097\/AUD.0000000000000121"},{"issue":"1","key":"3","doi-asserted-by":"crossref","first-page":"53","DOI":"10.3109\/03005368909077819","article-title":"Tinnitus--a study of its prevalence and characteristics","volume":"23","author":"A. Axelsson","year":"2009","journal-title":"British Journal of Audiology"},{"issue":"1","key":"4","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1159\/000431376","article-title":"Prevalence and determinants of tinnitus in the Italian adult population","volume":"45","author":"S. Gallus","year":"2015","journal-title":"Neuroepidemiology"},{"key":"5","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.cpr.2017.12.006","article-title":"A systematic review and meta-analysis of psychological functioning in chronic tinnitus","volume":"60","author":"K. J. Trevis","year":"2018","journal-title":"Clinical Psychology Review"},{"key":"6","doi-asserted-by":"publisher","DOI":"10.1002\/lary.26964"},{"issue":"2","key":"7","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1002\/lary.26107","article-title":"Relationships between tinnitus and the prevalence of anxiety and depression","volume":"127","author":"J. M. Bhatt","year":"2017","journal-title":"The Laryngoscope"},{"key":"8","doi-asserted-by":"publisher","DOI":"10.1007\/s10162-017-0642-8"},{"issue":"1","key":"9","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1080\/14992020500377089","article-title":"Long-term assessment of auditory changes resulting from a single noise exposure associated with non-occupational activities","volume":"45","author":"N. Schmuzigert","year":"2009","journal-title":"International Journal of Audiology"},{"issue":"6","key":"10","doi-asserted-by":"crossref","first-page":"3064","DOI":"10.1152\/jn.00319.2015","article-title":"Bimodal stimulus timing-dependent plasticity in primary auditory cortex is altered after noise exposure with and without tinnitus","volume":"114","author":"G. J. Basura","year":"2015","journal-title":"Journal of Neurophysiology"},{"issue":"6","key":"11","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1523\/JNEUROSCI.3960-15.2016","article-title":"Increased synchrony and bursting of dorsal cochlear nucleus fusiform cells correlate with tinnitus","volume":"36","author":"C. Wu","year":"2016","journal-title":"The Journal of Neuroscience"},{"key":"12","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2017.11.026"},{"key":"13","doi-asserted-by":"publisher","DOI":"10.1016\/j.heares.2017.04.016"},{"key":"14","doi-asserted-by":"publisher","DOI":"10.1037\/0735-7044.120.1.188"},{"issue":"3","key":"15","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1038\/nrneurol.2016.12","article-title":"Maladaptive plasticity in tinnitus--triggers, mechanisms and treatment","volume":"12","author":"S. E. Shore","year":"2016","journal-title":"Nature Reviews. Neurology"},{"key":"16","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.22036"},{"key":"17","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1219731110"},{"key":"18","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1707086114"},{"key":"19","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2016.03.016"},{"key":"20","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroimage.2009.01.069"},{"issue":"1-2","key":"21","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.heares.2009.03.002","article-title":"Acute high-intensity sound exposure alters responses of place cells in hippocampus","volume":"253","author":"T. J. Goble","year":"2009","journal-title":"Hearing Research"},{"key":"22","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0067778"},{"key":"23","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.heares.2016.09.010","article-title":"Acute high-intensity noise induces rapid Arc protein expression but fails to rapidly change GAD expression in amygdala and hippocampus of rats: effects of treatment with D-cycloserine","volume":"342","author":"M. R. Kapolowicz","year":"2016","journal-title":"Hearing Research"},{"key":"24","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2011.04.052"},{"key":"25","doi-asserted-by":"publisher","DOI":"10.1016\/j.nicl.2018.08.029"},{"issue":"2","key":"26","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0006-8993(86)90933-9","article-title":"Hippocampal responses evoked by tooth pulp and acoustic stimulation: depth profiles and effect of behavior","volume":"378","author":"J. Brankack","year":"1986","journal-title":"Brain Research"},{"issue":"4487","key":"27","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1126\/science.7466392","article-title":"Entorhinal and septal inputs differentially control sensory-evoked responses in the rat dentate gyrus","volume":"211","author":"S. A. Deadwyler","year":"1981","journal-title":"Science"},{"key":"28","first-page":"423","article-title":"Hippocampus","volume-title":"The Synaptic Organization of the Brain","author":"D. Johnston","year":"1998"},{"issue":"2","key":"29","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.tins.2003.11.005","article-title":"VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate","volume":"27","author":"R. T. Fremeau","year":"2004","journal-title":"Trends in Neurosciences"},{"key":"30","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0401764101"},{"issue":"3","key":"31","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1002\/cne.1037","article-title":"Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex","volume":"435","author":"F. Fujiyama","year":"2001","journal-title":"The Journal of Comparative Neurology"},{"key":"32","doi-asserted-by":"publisher","DOI":"10.1523\/jneurosci.4505-11.2012"},{"key":"33","doi-asserted-by":"publisher","DOI":"10.1523\/jneurosci.18-23-09733.1998"},{"key":"34","doi-asserted-by":"publisher","DOI":"10.1038\/39908"},{"key":"35","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2014.06.023"},{"key":"36","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2014.04.014"},{"key":"37","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.eplepsyres.2014.10.003","article-title":"Chronic stress shifts the GABA reversal potential in the hippocampus and increases seizure susceptibility","volume":"109","author":"G. MacKenzie","year":"2015","journal-title":"Epilepsy Research"},{"key":"38","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1313505110"},{"key":"39","doi-asserted-by":"publisher","DOI":"10.1001\/jamapsychiatry.2015.49"},{"key":"40","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0703806104"},{"key":"41","doi-asserted-by":"publisher","DOI":"10.1038\/nature11356"},{"key":"42","doi-asserted-by":"publisher","DOI":"10.1038\/nature09582"},{"issue":"2","key":"43","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1539\/joh.L8084","article-title":"Effects of chronic noise exposure on spatial learning and memory of rats in relation to neurotransmitters and NMDAR2B alteration in the hippocampus","volume":"51","author":"B. Cui","year":"2009","journal-title":"Journal of Occupational Health"},{"key":"44","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.aal3175"},{"issue":"8","key":"45","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1002\/hipo.23058","article-title":"Remodeling of cholinergic input to the hippocampus after noise exposure and tinnitus induction in guinea pigs","volume":"29","author":"L. Zhang","year":"2019","journal-title":"Hippocampus"},{"key":"46","doi-asserted-by":"publisher","DOI":"10.1016\/j.jneumeth.2012.12.023"},{"key":"47","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/j.neubiorev.2017.03.009","article-title":"Acoustic startle modification as a tool for evaluating auditory function of the mouse: progress, pitfalls, and potential","volume":"77","author":"A. M. Lauer","year":"2017","journal-title":"Neuroscience and Biobehavioral Reviews"},{"key":"48","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.heares.2017.01.003","article-title":"Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms","volume":"349","author":"M. C. Liberman","year":"2017","journal-title":"Hearing Research"},{"key":"49","doi-asserted-by":"publisher","DOI":"10.1523\/jneurosci.2598-12.2012"},{"issue":"4","key":"50","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/j.otc.2020.03.006","article-title":"Does tinnitus fill in the gap using electrophysiology? A scoping review","volume":"53","author":"V. Duda","year":"2020","journal-title":"Otolaryngologic Clinics of North America"},{"key":"51","doi-asserted-by":"publisher","DOI":"10.1002\/cne.20354"},{"key":"52","doi-asserted-by":"publisher","DOI":"10.1523\/jneurosci.21-22-j0001.2001"},{"key":"53","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuron.2011.02.002"},{"key":"54","doi-asserted-by":"publisher","DOI":"10.1016\/s0896-6273(01)00344-0"},{"issue":"3","key":"55","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/S0959-4388(03)00078-3","article-title":"Presynaptic control of quantal size: kinetic mechanisms and implications for synaptic transmission and plasticity","volume":"13","author":"G. Liu","year":"2003","journal-title":"Current Opinion in Neurobiology"},{"issue":"12","key":"56","doi-asserted-by":"crossref","first-page":"5607","DOI":"10.1073\/pnas.91.12.5607","article-title":"Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter","volume":"91","author":"B. Ni","year":"1994","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"issue":"8","key":"57","doi-asserted-by":"crossref","first-page":"5789","DOI":"10.1523\/JNEUROSCI.15-08-05789.1995","article-title":"Regional expression and cellular localization of the Na(+)-dependent inorganic phosphate cotransporter of rat brain","volume":"15","author":"B. Ni","year":"1995","journal-title":"The Journal of Neuroscience"},{"key":"58","doi-asserted-by":"publisher","DOI":"10.1002\/hipo.20006"},{"key":"59","doi-asserted-by":"publisher","DOI":"10.1016\/j.brainres.2011.08.035"},{"issue":"12","key":"60","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1023\/A:1026606201069","article-title":"Restraint stress-induced alterations in the levels of biogenic amines, amino acids, and AChE activity in the hippocampus","volume":"25","author":"B. S. S. Rao","year":"2000","journal-title":"Neurochemical Research"},{"key":"61","doi-asserted-by":"publisher","DOI":"10.1046\/j.1471-4159.2000.0742622.x"},{"key":"62","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2018.09.008"},{"issue":"7363","key":"63","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/nature10360","article-title":"Neocortical excitation\/inhibition balance in information processing and social dysfunction","volume":"477","author":"O. Yizhar","year":"2011","journal-title":"Nature"},{"issue":"2","key":"64","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/hipo.22360","article-title":"Excitation\/inhibition imbalance and impaired synaptic inhibition in hippocampal area CA3 of Mecp2 knockout mice","volume":"25","author":"G. Calfa","year":"2015","journal-title":"Hippocampus"},{"issue":"4","key":"65","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1002\/1098-1063(2000)10:4<398::AID-HIPO6>3.0.CO;2-K","article-title":"Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways","volume":"10","author":"M. P. Witter","year":"2000","journal-title":"Hippocampus"},{"issue":"3","key":"66","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1002\/cne.902640306","article-title":"The entorhinal cortex of the monkey: II. Cortical afferents","volume":"264","author":"R. Insausti","year":"1987","journal-title":"The Journal of Comparative Neurology"},{"issue":"2","key":"67","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1002\/(SICI)1096-9861(19980824)398:2<179::AID-CNE3>3.0.CO;2-Y","article-title":"Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat","volume":"398","author":"R. D. Burwell","year":"1998","journal-title":"The Journal of Comparative Neurology"},{"issue":"2","key":"68","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1016\/j.neuron.2017.12.010","article-title":"A non-canonical reticular-limbic central auditory pathway via medial septum contributes to fear conditioning","volume":"97","author":"G.-W. Zhang","year":"2018","journal-title":"Neuron"},{"issue":"1","key":"69","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainresrev.2007.05.002","article-title":"Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex","volume":"56","author":"L. A. Cenquizca","year":"2007","journal-title":"Brain Research Reviews"},{"issue":"8","key":"70","doi-asserted-by":"crossref","first-page":"9952","DOI":"10.3390\/ijerph120809952","article-title":"The association between noise, cortisol and heart rate in a small-scale gold mining community-a pilot study","volume":"12","author":"A. Green","year":"2015","journal-title":"International Journal of Environmental Research and Public Health"},{"issue":"10","key":"71","first-page":"657","article-title":"Effect of acute noise exposure on salivary cortisol: a randomized controlled trial","volume":"54","author":"G. Pouryaghoub","year":"2016","journal-title":"Acta Medica Iranica"},{"key":"72","doi-asserted-by":"publisher","DOI":"10.1016\/j.neulet.2006.01.037"},{"issue":"4","key":"73","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1515\/revneuro-2015-0042","article-title":"Chronic stress, hippocampus and parvalbumin-positive interneurons: what do we know so far?","volume":"27","author":"I. Zaletel","year":"2016","journal-title":"Reviews in the Neurosciences"},{"issue":"73","key":"74","doi-asserted-by":"crossref","first-page":"343","DOI":"10.4103\/1463-1741.144394","article-title":"Chronic noise stress-induced alterations of glutamate and gamma-aminobutyric acid and their metabolism in the rat brain","volume":"16","author":"A. I. Kazi","year":"2014","journal-title":"Noise & Health"},{"issue":"3","key":"75","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1152\/jn.00457.2014","article-title":"Stimulus-timing-dependent modifications of rate-level functions in animals with and without tinnitus","volume":"113","author":"R. A. Stefanescu","year":"2015","journal-title":"Journal of Neurophysiology"},{"issue":"2","key":"76","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s00405-014-3479-3","article-title":"Expression of immediate-early genes in the dorsal cochlear nucleus in salicylate-induced tinnitus","volume":"273","author":"S.-S. Hu","year":"2016","journal-title":"European Archives of Oto-Rhino-Laryngology"},{"issue":"6","key":"77","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1016\/j.neuron.2010.04.032","article-title":"Tuning out the noise: limbic-auditory interactions in tinnitus","volume":"66","author":"J. P. Rauschecker","year":"2010","journal-title":"Neuron"},{"issue":"4","key":"78","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1007\/s00221-003-1747-3","article-title":"CNS somatosensory-auditory interactions elicit or modulate tinnitus","volume":"153","author":"R. A. Levine","year":"2003","journal-title":"Experimental Brain Research"},{"issue":"6","key":"79","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1159\/000452472","article-title":"Somatosensory tinnitus: correlation between cranio-cervico-mandibular disorder history and somatic modulation","volume":"21","author":"M. Ralli","year":"2016","journal-title":"Audiology & Neuro-Otology"},{"issue":"6","key":"80","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1159\/000066155","article-title":"The influence of voluntary muscle contractions upon the onset and modulation of tinnitus","volume":"7","author":"T. G. Sanchez","year":"2002","journal-title":"Audiology & Neuro-Otology"},{"issue":"1","key":"81","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1002\/hipo.10037","article-title":"The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation","volume":"13","author":"T. van Groen","year":"2003","journal-title":"Hippocampus"},{"issue":"2","key":"82","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1097\/00006199-200103000-00003","article-title":"Effects of entorhinal cortex lesions on sensory integration and spatial learning","volume":"50","author":"A. E. Davis","year":"2001","journal-title":"Nursing Research"}],"container-title":["Neural Plasticity"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/downloads.hindawi.com\/journals\/np\/2021\/8833087.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/downloads.hindawi.com\/journals\/np\/2021\/8833087.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/downloads.hindawi.com\/journals\/np\/2021\/8833087.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,17]],"date-time":"2023-10-17T17:15:00Z","timestamp":1697562900000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.hindawi.com\/journals\/np\/2021\/8833087\/"}},"subtitle":[],"editor":[{"given":"Josef","family":"Syka","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2021,1,14]]},"references-count":82,"alternative-id":["8833087","8833087"],"URL":"https:\/\/doi.org\/10.1155\/2021\/8833087","relation":{},"ISSN":["1687-5443","2090-5904"],"issn-type":[{"value":"1687-5443","type":"electronic"},{"value":"2090-5904","type":"print"}],"subject":[],"published":{"date-parts":[[2021,1,14]]}}}