{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,28]],"date-time":"2026-08-28T04:18:06Z","timestamp":1787890686122,"version":"build-2784847793"},"reference-count":87,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T00:00:00Z","timestamp":1787529600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000025","name":"National Institute of Mental Health","doi-asserted-by":"publisher","award":["R01MH135565"],"award-info":[{"award-number":["R01MH135565"]}],"id":[{"id":"10.13039\/100000025","id-type":"DOI","asserted-by":"publisher"}]},{"award":["R01MH135565"],"award-info":[{"award-number":["R01MH135565"]}],"id":[{"id":"https:\/\/ror.org\/04xeg9z08","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000065","name":"National Institute of Neurological Disorders and Stroke","doi-asserted-by":"publisher","award":["R01NS118440"],"award-info":[{"award-number":["R01NS118440"]}],"id":[{"id":"10.13039\/100000065","id-type":"DOI","asserted-by":"publisher"}]},{"award":["R01NS118440"],"award-info":[{"award-number":["R01NS118440"]}],"id":[{"id":"https:\/\/ror.org\/01s5ya894","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32GM150581"],"award-info":[{"award-number":["T32GM150581"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"award":["T32GM150581"],"award-info":[{"award-number":["T32GM150581"]}],"id":[{"id":"https:\/\/ror.org\/04q48ey07","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Accurate and efficient memory processing is essential for survival. A body of ongoing work in both human subjects and animal models suggests that memory processing may differ substantially between males and females. In mice, contextual fear memory (CFM) encoding, consolidation, and recall have been well studied, and the mouse hippocampus and amygdala have been implicated in these processes. The present pilot study addresses whether the activation of these brain regions differs substantially between male and female mice at each stage of CFM processing. We find that male and female mice show no differences in sleep behavior, which is essential for CFM consolidation, following single-trial contextual fear conditioning (CFC). We also find no significant differences in CFM recall performance between male and female mice. However, females show a trend for larger increases in CA1 cFos expression, relative to males, during CFM encoding. On the other hand, only males\u2014but not females\u2014show an apparent increase in cFos expression among dentate gyrus (DG) granule cells during CFM consolidation. Males also show a trend for a larger apparent reduction in cFos in CA1 and CA3 during CFM consolidation, relative to females. These preliminary findings highlight the idea that the neurobiological underpinnings of memory processing may differ between males and females, even when performance during recall is identical.<\/jats:p>","DOI":"10.3390\/cells15171523","type":"journal-article","created":{"date-parts":[[2026,8,24]],"date-time":"2026-08-24T14:49:34Z","timestamp":1787582974000},"page":"1523","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Male and Female Mice Show Similar Fear Memory Performance Despite Hippocampal Immediate Early Gene Expression Differences During Encoding and Consolidation"],"prefix":"10.3390","volume":"15","author":[{"given":"Katherine O.","family":"McDonald","sequence":"first","affiliation":[{"name":"Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Temmie","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aditi","family":"Prabhu","sequence":"additional","affiliation":[{"name":"Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2921-0509","authenticated-orcid":false,"given":"Sara J.","family":"Aton","sequence":"additional","affiliation":[{"name":"Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,8,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/j.neubiorev.2010.07.002","article-title":"Sex bias in neuroscience and biomedical research","volume":"35","author":"Beery","year":"2011","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.cobeha.2018.04.005","article-title":"Focus on females: A less biased approach for studying strategies and mechanisms of memory","volume":"23","author":"Tronson","year":"2018","journal-title":"Curr. Opin. Behav. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/j.ncl.2023.01.001","article-title":"Sex Differences in Alzheimer\u2019s Disease","volume":"41","author":"Aggarwal","year":"2023","journal-title":"Neurol. Clin."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.3233\/JAD-180141","article-title":"Differences Between Women and Men in Incidence Rates of Dementia and Alzheimer\u2019s Disease","volume":"64","author":"Beam","year":"2018","journal-title":"J. Alzheimer\u2019s Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2765","DOI":"10.1038\/s41467-023-38374-z","article-title":"Functional variants identify sex-specific genes and pathways in Alzheimer\u2019s Disease","volume":"14","author":"Bourquard","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2541","DOI":"10.1093\/brain\/awac177","article-title":"Sex differences in the genetic architecture of cognitive resilience to Alzheimer\u2019s disease","volume":"145","author":"Eissman","year":"2022","journal-title":"Brain"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1098\/rstb.1997.0132","article-title":"Hierarchical organization of cognitive memory","volume":"352","author":"Mishkin","year":"1997","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1038\/nn834","article-title":"Critical role of the hippocampus in memory for sequences of events","volume":"5","author":"Fortin","year":"2002","journal-title":"Nat. Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/S0166-4328(99)00044-3","article-title":"The hippocampus and mechanisms of declarative memory","volume":"103","author":"Eichenbaum","year":"1999","journal-title":"Behav. Brain Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1111\/j.1469-7580.2005.00421.x","article-title":"Functional neuroanatomy of remote episodic, semantic and spatial memory: A unified account based on multiple trace theory","volume":"207","author":"Moscovitch","year":"2005","journal-title":"J. Anat."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nrn3945","article-title":"Neuronal circuits for fear and anxiety","volume":"16","author":"Tovote","year":"2015","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1382","DOI":"10.1038\/s41467-020-15121-2","article-title":"Encoding of contextual fear memory in hippocampal-amygdala circuit","volume":"11","author":"Kim","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1101\/lm.81905","article-title":"Encoding, consolidation, and retrieval of contextual memory: Differential involvement of dorsal CA3 and CA1 hippocampal subregions","volume":"12","author":"Daumas","year":"2005","journal-title":"Learn. Mem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"5507","DOI":"10.1007\/s12035-018-1463-4","article-title":"Hippocampus and Prefrontal Cortex Modulation of Contextual Fear Memory Is Dissociated by Inhibiting De Novo Transcription During Late Consolidation","volume":"56","author":"Pereira","year":"2019","journal-title":"Mol. Neurobiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"109408","DOI":"10.1016\/j.isci.2024.109408","article-title":"Sleep-dependent engram reactivation during hippocampal memory consolidation associated with subregion-specific biosynthetic changes","volume":"27","author":"Wang","year":"2024","journal-title":"iScience"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"ra41","DOI":"10.1126\/scisignal.aad4949","article-title":"Sleep deprivation impairs memory by attenuating mTORC1-dependent protein synthesis","volume":"9","author":"Tudor","year":"2016","journal-title":"Sci. Signal."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"6781","DOI":"10.1523\/JNEUROSCI.22-15-06781.2002","article-title":"Two time periods of hippocampal mRNA synthesis are required for memory consolidation of fear-motivated learning","volume":"22","author":"Igaz","year":"2002","journal-title":"J. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1101\/lm.5.4.365","article-title":"Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA","volume":"5","author":"Bourtchouladze","year":"1998","journal-title":"Learn. Mem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3711","DOI":"10.1093\/cercor\/bhy174","article-title":"Hippocampal Network Oscillations Rescue Memory Consolidation Deficits Caused by Sleep Loss","volume":"28","author":"Ognjanovski","year":"2018","journal-title":"Cereb. Cortex"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"15039","DOI":"10.1038\/ncomms15039","article-title":"Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation","volume":"8","author":"Ognjanovski","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3389\/fnsys.2014.00061","article-title":"CA1 hippocampal network activity changes during sleep-dependent memory consolidation","volume":"8","author":"Ognjanovski","year":"2014","journal-title":"Front. Syst. Neurosci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e27868","DOI":"10.7554\/eLife.27868","article-title":"Parvalbumin-positive interneurons mediate neocortical-hippocampal interactions that are necessary for memory consolidation","volume":"6","author":"Xia","year":"2017","journal-title":"eLife"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1122","DOI":"10.1038\/nature08488","article-title":"Sleep deprivation impairs cAMP signalling in the hippocampus","volume":"461","author":"Vecsey","year":"2009","journal-title":"Nature"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e13424","DOI":"10.7554\/eLife.13424","article-title":"Sleep deprivation causes memory deficits by negatively impacting neuronal connectivity in hippocampal area CA1","volume":"5","author":"Havekes","year":"2016","journal-title":"eLife"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e2108534118","DOI":"10.1073\/pnas.2108534118","article-title":"Hippocampal neurons\u2019 cytosolic and membrane-bound ribosomal transcript profiles are differentially regulated by learning and subsequent sleep","volume":"118","author":"Delorme","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.nlm.2018.04.006","article-title":"Sleep loss disrupts Arc expression in dentate gyrus neurons","volume":"160","author":"Delorme","year":"2019","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1038\/s41467-022-29384-4","article-title":"Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions","volume":"13","author":"Roy","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.neubiorev.2014.01.001","article-title":"Female mice liberated for inclusion in neuroscience and biomedical research","volume":"40","author":"Prendergast","year":"2014","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1038\/npp.2016.174","article-title":"Sex Differences in Context Fear Generalization and Recruitment of Hippocampus and Amygdala during Retrieval","volume":"42","author":"Keiser","year":"2016","journal-title":"Neuropsychopharmacology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"a054081","DOI":"10.1101\/lm.054081.124","article-title":"Multiple context discrimination in adult rats: Sex variability and dynamics of time-dependent generalization of an aversive memory","volume":"32","year":"2025","journal-title":"Learn. Mem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.neuroscience.2009.01.009","article-title":"Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation","volume":"159","author":"Gresack","year":"2009","journal-title":"Neuroscience"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1101\/lm.053471.121","article-title":"Developmental emergence of persistent memory for contextual and auditory fear in mice","volume":"28","author":"Samifanni","year":"2021","journal-title":"Learn. Mem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1101\/lm.48803","article-title":"Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning","volume":"10","author":"Graves","year":"2003","journal-title":"Learn. Mem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"zsz289","DOI":"10.1093\/sleep\/zsz289","article-title":"Sex differences within sleep in gonadally intact rats","volume":"43","author":"Swift","year":"2020","journal-title":"Sleep"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"23622","DOI":"10.1038\/s41598-024-70996-1","article-title":"The importance of including both sexes in preclinical sleep studies and analyses","volume":"14","author":"Mannino","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Choi, J., Kim, S., Fujiyama, T., Miyoshi, C., Park, M., Suzuki-Abe, H., Yanagisawa, M., and Funato, H. (2021). The Role of Reproductive Hormones in Sex Differences in Sleep Homeostasis and Arousal Response in Mice. Front. Neurosci., 15.","DOI":"10.3389\/fnins.2021.739236"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"105688","DOI":"10.1016\/j.psyneuen.2022.105688","article-title":"The role of the cannabinoid system in fear memory and extinction in male and female mice","volume":"138","author":"Mizuno","year":"2022","journal-title":"Psychoneuroendocrinology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"108127","DOI":"10.1016\/j.nlm.2025.108127","article-title":"Reductions in protein degradation in the retrosplenial cortex regulate contextual fear memory formation in a sex-independent manner","volume":"223","author":"Turner","year":"2026","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1101\/lm.053429.121","article-title":"Females, but not males, require protein degradation in the hippocampus for contextual fear memory formation","volume":"28","author":"Martin","year":"2021","journal-title":"Learn. Mem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1016\/j.tins.2019.07.009","article-title":"A Dynamic Memory Systems Framework for Sex Differences in Fear Memory","volume":"42","author":"Tronson","year":"2019","journal-title":"Trends Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"115480","DOI":"10.1016\/j.bbr.2025.115480","article-title":"Experimenters\u2019 sex modulates anxiety-like behavior, contextual fear, and microglial oxytocin transcription in mice","volume":"483","author":"Sakai","year":"2025","journal-title":"Behav. Brain Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1186\/s13041-021-00798-3","article-title":"In vivo imaging of immediate early gene expression dynamics segregates neuronal ensemble of memories of dual events","volume":"14","author":"Meenakshi","year":"2021","journal-title":"Mol. Brain"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3389\/fncel.2015.00072","article-title":"The pattern of c-Fos expression and its refractory period in the brain of rats and monkeys","volume":"9","author":"Barros","year":"2015","journal-title":"Front. Cell Neurosci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/0304-3940(89)90381-9","article-title":"Proto-oncogene c-fos is transiently induced in the rat cerebral cortex after forebrain","volume":"98","author":"Onodera","year":"1989","journal-title":"Ischemia Neurosci. Lett."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Schoenenberger, P., Gerosa, D., and Oertner, T. (2009). Temporal Control of Immediate Early Gene Induction by Light. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0008185"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e2019318118","DOI":"10.1073\/pnas.2019318118","article-title":"Sleep loss drives acetylcholine- and somatostatin interneuron-mediated gating of hippocampal activity, to inhibit memory consolidation","volume":"118","author":"Delorme","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_47","first-page":"46","article-title":"Circadian Oscillations within the Hippocampus Support Memory Formation and Persistence","volume":"5","year":"2012","journal-title":"Front. Mol. Neurosci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"eaea3381","DOI":"10.1126\/science.aea3381","article-title":"A whole-brain single-cell atlas of circadian neural activity in mice","volume":"391","author":"Yamashita","year":"2025","journal-title":"Science"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"zsac301","DOI":"10.1093\/sleep\/zsac301","article-title":"Atypical hypnotic compound ML297 restores sleep architecture immediately following emotionally valenced learning, to promote memory consolidation and hippocampal network activation during recall","volume":"46","author":"Martinez","year":"2023","journal-title":"Sleep"},{"key":"ref_50","first-page":"325","article-title":"Repeated Collection of Vaginal Smear Causes Stress in Mice","volume":"59","author":"Varol","year":"2022","journal-title":"Noro. Psikiyatr. Ars."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Byers, S., Wiles, M., Dunn, S., and Taft, R. (2012). Mouse Estrous Cycle Identification Tool and Images. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0035538"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"115067","DOI":"10.1016\/j.isci.2026.115067","article-title":"Dentate gyrus network regulation by somatostatin- and parvalbumin-expressing interneurons differentially impacts hippocampal spatial memory processing","volume":"29","author":"Raven","year":"2026","journal-title":"iScience"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1016\/j.nlm.2013.11.021","article-title":"Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory","volume":"109","author":"Prince","year":"2014","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1016\/j.neuron.2014.07.017","article-title":"Neurons Are Recruited to a Memory Trace Based on Relative Neuronal Excitability Immediately before Training","volume":"83","author":"Yiu","year":"2014","journal-title":"Neuron"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"107044","DOI":"10.1016\/j.nlm.2019.107044","article-title":"Modulation of CA2 neuronal activity increases behavioral responses to fear conditioning in female mice","volume":"163","author":"Alexander","year":"2019","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1016\/j.physbeh.2011.12.016","article-title":"Role of gonadal hormones in anxiety and fear memory formation and inhibition in male mice","volume":"105","author":"McDermott","year":"2012","journal-title":"Physiol. Behav."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.nlm.2014.12.009","article-title":"Estradiol replacement enhances fear memory formation, impairs extinction and reduces COMT expression levels in the hippocampus of ovariectomized female mice","volume":"118","author":"McDermott","year":"2015","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.neulet.2018.09.030","article-title":"Sex differences in the effects of adult short-term isolation rearing on contextual fear memory and extinction","volume":"687","author":"Matsuda","year":"2018","journal-title":"Neurosci. Lett."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1038\/nn.3614","article-title":"Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits","volume":"17","author":"Kohara","year":"2014","journal-title":"Nat. Neurosci."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1844","DOI":"10.1002\/cne.23263","article-title":"Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus","volume":"521","author":"Cui","year":"2013","journal-title":"J. Comp. Neurol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"12025","DOI":"10.1523\/JNEUROSCI.4094-07.2007","article-title":"Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons","volume":"27","author":"Zhao","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2193","DOI":"10.1038\/s41593-024-01771-8","article-title":"The hippocampal CA2 region discriminates social threat from social safety","volume":"27","author":"Kassraian","year":"2024","journal-title":"Nat. Neurosci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/nature13028","article-title":"The hippocampal CA2 region is essential for social memory","volume":"508","author":"Hitti","year":"2014","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"233","DOI":"10.3389\/fnbeh.2019.00233","article-title":"Social Memory and the Role of the Hippocampal CA2 Region","volume":"13","author":"Tzakis","year":"2019","journal-title":"Front. Behav. Neurosci."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.neubiorev.2021.03.020","article-title":"CA2 beyond social memory: Evidence for a fundamental role in hippocampal information processing","volume":"126","author":"Lehr","year":"2021","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1126\/science.1239073","article-title":"Creating a false memory in the hippocampus","volume":"341","author":"Ramirez","year":"2013","journal-title":"Science"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/nature11028","article-title":"Optogenetic stimulation of a hippocampal engram activates fear memory recall","volume":"484","author":"Liu","year":"2012","journal-title":"Nature"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1016\/j.neuron.2016.01.024","article-title":"Hippocampal Somatostatin Interneurons Control the Size of Neuronal Memory Ensembles","volume":"89","author":"Stefanelli","year":"2016","journal-title":"Neuron"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"e13090","DOI":"10.1111\/jne.13090","article-title":"Sex-dependent responsiveness of hippocampal neurons to sex neurosteroids: A role of Arc\/Arg3","volume":"34","author":"Brokling","year":"2022","journal-title":"J. Neuroendocrinol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1038\/s42003-025-08856-5","article-title":"Immediate-early genes Arc and c-Fos show divergent brain-wide expression following contextual fear conditioning","volume":"8","author":"Bulthuis","year":"2025","journal-title":"Commun. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.conb.2020.03.004","article-title":"Parallel processing streams in the hippocampus","volume":"64","author":"Lee","year":"2020","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Satchell, M., Butel-Fry, E., Zoureddine, Z., Simmons, A., Ognjanovski, N., Aton, S., and Zochowski, M. (2025). Cholinergic modulation of neural networks supports sequential and complementary roles for NREM and REM states in memory consolidation. PLoS Comput. Biol., 21.","DOI":"10.1371\/journal.pcbi.1013097"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.neulet.2018.05.024","article-title":"Gender dependent contribution of muscarinic receptors in memory retrieval under sub-chronic stress","volume":"681","author":"Rashid","year":"2018","journal-title":"Neurosci. Lett."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"105776","DOI":"10.1016\/j.psyneuen.2022.105776","article-title":"Estrous cycle contributes to state-dependent contextual fear in female rats","volume":"141","author":"Blair","year":"2022","journal-title":"Psychoneuroendocrinology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/j.physbeh.2016.05.026","article-title":"Sex differences and estrous cycle effects on foreground contextual fear conditioning","volume":"163","author":"Cossio","year":"2016","journal-title":"Physiol. Behav."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"11","DOI":"10.2174\/1876386300902010011","article-title":"c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury?","volume":"2","author":"Gao","year":"2009","journal-title":"Open Pain J."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1016\/j.cell.2020.02.055","article-title":"Functionally Distinct Neuronal Ensembles within the Memory Engram","volume":"181","author":"Sun","year":"2020","journal-title":"Cell"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"119689","DOI":"10.1016\/j.neuroimage.2022.119689","article-title":"Exogenous estradiol and oxytocin modulate sex differences in hippocampal reactivity during the encoding of episodic","volume":"264","author":"Coenjaerts","year":"2022","journal-title":"Neuroimage"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"3320","DOI":"10.1002\/hbm.22144","article-title":"Functional neuroimaging of sex differences in autobiographical memory recall","volume":"34","author":"Young","year":"2013","journal-title":"Hum. Brain Mapp."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"14200","DOI":"10.1073\/pnas.0601648103","article-title":"The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory","volume":"103","author":"Mackiewicz","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1212\/WNL.0000000000002570","article-title":"For the Alzheimer\u2019s Disease Neuroimaging Initiative. Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy","volume":"86","author":"Sundermann","year":"2016","journal-title":"Neurology"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.nlm.2014.02.003","article-title":"Sex differences in extinction recall in posttraumatic stress disorder: A pilot fMRI study","volume":"113","author":"Shvil","year":"2014","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Landemard, A., Krumin, M., Harris, K., and Carandini, M. (2026). Brainwide blood volume reflects opposing neural populations. Nature.","DOI":"10.1038\/s41586-026-10350-9"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"461","DOI":"10.2466\/04.22.24.27.PMS.113.5.461-480","article-title":"A preliminary study of sex differences in brain activation during a spatial navigation task in healthy adults","volume":"113","author":"Sneider","year":"2011","journal-title":"Percept. Mot. Ski."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.neuroimage.2015.04.013","article-title":"Developmental sex differences in resting state functional connectivity of amygdala sub-regions","volume":"115","author":"Alarcon","year":"2015","journal-title":"Neuroimage"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"6139","DOI":"10.1093\/cercor\/bhac491","article-title":"Sex differences in default mode network connectivity in healthy aging adults","volume":"33","author":"Horien","year":"2023","journal-title":"Cereb. Cortex"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1001\/archpsyc.1996.01830070031007","article-title":"Sex differences in human brain morphometry and metabolism: An in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging","volume":"53","author":"Murphy","year":"1996","journal-title":"Arch. Gen. Psychiatry"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/15\/17\/1523\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,28]],"date-time":"2026-08-28T04:11:25Z","timestamp":1787890285000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/15\/17\/1523"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,24]]},"references-count":87,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["cells15171523"],"URL":"https:\/\/doi.org\/10.3390\/cells15171523","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,24]]}}}