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Current Alzheimer Research

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ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

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Research Article

Effect of APOE4 Allele and Gender on the Rate of Atrophy in the Hippocampus, Entorhinal Cortex, and Fusiform Gyrus in Alzheimer’s Disease

Author(s): Eid Abo Hamza, Ahmed A. Moustafa*, Richard Tindle, Rasu Karki, Shahed Nalla, Mohamed S. Hamid and Mohamad EL HAJ

Volume 19, Issue 14, 2022

Published on: 15 March, 2023

Page: [943 - 953] Pages: 11

DOI: 10.2174/1567205020666230309113749

Price: $65

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Abstract

Background: The hippocampus, entorhinal cortex, and fusiform gyrus are brain areas that deteriorate during early-stage Alzheimer’s disease (AD). The ApoE4 allele has been identified as a risk factor for AD development, is linked to an increase in the aggregation of amyloid β (Aβ) plaques in the brain, and is responsible for atrophy of the hippocampal area. However, to our knowledge, the rate of deterioration over time in individuals with AD, with or without the ApoE4 allele, has not been investigated.

Methods: In this study, we, for the first time, analyze atrophy in these brain structures in AD patients with and without the ApoE4 using the Alzheimer’s Disease Neuroimaging Initiative (ADNI) dataset.

Results: It was found that the rate of decrease in the volume of these brain areas over 12 months was related to the presence of ApoE4. Further, we found that neural atrophy was not different for female and male patients, unlike prior studies, suggesting that the presence of ApoE4 is not linked to the gender difference in AD.

Conclusion: Our results confirm and extend previous findings, showing that the ApoE4 allele gradually impacts brain regions impacted by AD.

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[1]
Velayudhan, L.; Proitsi, P.; Westman, E.; Muehlboeck, J.S.; Mecocci, P.; Vellas, B.; Tsolaki, M. Kłoszewska, I.; Soininen, H.; Spenger, C.; Hodges, A.; Powell, J.; Lovestone, S.; Simmons, A. Entorhinal cortex thickness predicts cognitive decline in Alzheimer’s disease. J. Alzheimers Dis., 2013, 33(3), 755-766.
[http://dx.doi.org/10.3233/JAD-2012-121408] [PMID: 23047370]
[2]
Cao, L.; Wang, H.F.; Tan, L.; Sun, F.R.; Tan, M.S.; Tan, C.C.; Jiang, T.; Yu, J.T.; Tan, L. Effect of HMGCR genetic variation on neuroim-aging biomarkers in healthy, mild cognitive impairment and Alzheimer’s disease cohorts. Oncotarget, 2016, 7(12), 13319-13327.
[http://dx.doi.org/10.18632/oncotarget.7797] [PMID: 26950278]
[3]
Pensalfini, A.; Albay, R., III; Rasool, S.; Wu, J.W.; Hatami, A.; Arai, H.; Margol, L.; Milton, S.; Poon, W.W.; Corrada, M.M.; Kawas, C.H.; Glabe, C.G. Intracellular amyloid and the neuronal origin of Alzheimer neuritic plaques. Neurobiol. Dis., 2014, 71, 53-61.
[http://dx.doi.org/10.1016/j.nbd.2014.07.011] [PMID: 25092575]
[4]
Moustafa, A.A.; Hassan, M.; Hewedi, D.H.; Hewedi, I.; Garami, J.K.; Al Ashwal, H.; Zaki, N.; Seo, S.Y.; Cutsuridis, V.; Angulo, S.L.; Natesh, J.Y.; Herzallah, M.M.; Frydecka, D.; Misiak, B.; Salama, M.; Mohamed, W.; El Haj, M.; Hornberger, M. Genetic underpinnings in Alzheimer’s disease-a review. Rev. Neurosci., 2017, 29(1), 21-38.
[http://dx.doi.org/10.1515/revneuro-2017-0036] [PMID: 28949931]
[5]
Moustafa, A.A. Alzheimer’s Disease: Understanding Biomarkers, Big Data, and Therapy; Elsevier: Amsterdam, 2021.
[6]
Fiorilli, J.; Bos, J.J.; Grande, X.; Lim, J.; Düzel, E.; Pennartz, C.M.A. Reconciling the object and spatial processing views of the perirhinal cortex through task‐relevant unitization. Hippocampus, 2021, 31(7), 737-755.
[http://dx.doi.org/10.1002/hipo.23304] [PMID: 33523577]
[7]
Ito, R.; Robbins, T.W.; Pennartz, C.M.; Everitt, B.J. Functional interaction between the hippocampus and nucleus accumbens shell is nec-essary for the acquisition of appetitive spatial context conditioning. J. Neurosci., 2008, 28(27), 6950-6959.
[http://dx.doi.org/10.1523/JNEUROSCI.1615-08.2008] [PMID: 18596169]
[8]
Jankowski, M.M.; Ronnqvist, K.C.; Tsanov, M.; Vann, S.D.; Wright, N.F.; Erichsen, J.T.; Aggleton, J.P.; O’Mara, S.M. The anterior thala-mus provides a subcortical circuit supporting memory and spatial navigation. Front. Syst. Neurosci., 2013, 7, 45.
[http://dx.doi.org/10.3389/fnsys.2013.00045] [PMID: 24009563]
[9]
Yoo, H.B.; Umbach, G.; Lega, B. Neurons in the human medial temporal lobe track multiple temporal contexts during episodic memory processing. Neuroimage, 2021, 245, 118689.
[http://dx.doi.org/10.1016/j.neuroimage.2021.118689] [PMID: 34742943]
[10]
Zheng, J.; Schjetnan, A.G.P.; Yebra, M.; Mosher, C.; Kalia, S.; Valiante, T.A. Cognitive boundary signals in the human medial temporal lobe shape episodic memory representation. 2021. Nat. Neurosci., 2022, 25, 358-368.
[http://dx.doi.org/10.1101/2021.01.16.426538]
[11]
Zheng, J.; Schjetnan, A.G.; Yebra, M.; Gomes, B.A.; Mosher, C.P.; Kalia, S.K. Neurons detect cognitive boundaries to structure episodic memo-ries in humans. Nat. Neurosci., 2022, 25, 358-368.
[12]
Mulders, P; Jaarsveld, S; Tendolkar, I; Eijndhoven, P Electroconvulsive therapy for depression: Neurobiological mechanisms. Neurobiol. Depress., 2019, 361-73. INCOMPLETE
[13]
Eriksson, P. Nerve Cells and Memory. Encyclopedia of the brain; Elsevier: Amsterdam, 2002.
[http://dx.doi.org/10.1016/B0-12-227210-2/00232-6]
[14]
Bellgowan, P.S.F.; Buffalo, E.A.; Bodurka, J.; Martin, A. Lateralized spatial and object memory encoding in entorhinal and perirhinal corti-ces. Learn. Mem., 2009, 16(7), 433-438.
[http://dx.doi.org/10.1101/lm.1357309] [PMID: 19553381]
[15]
Takehara-Nishiuchi, K. Entorhinal cortex and consolidated memory. Neurosci. Res., 2014, 84, 27-33.
[http://dx.doi.org/10.1016/j.neures.2014.02.012] [PMID: 24642278]
[16]
Suter, E.E.; Weiss, C.; Disterhoft, J.F. Differential responsivity of neurons in perirhinal cortex, lateral entorhinal cortex, and dentate gyrus during time‐bridging learning. Hippocampus, 2019, 29(6), 511-526.
[http://dx.doi.org/10.1002/hipo.23041] [PMID: 30311282]
[17]
Olajide, O.J.; Suvanto, M.E. Chapman, CAJBO Molecular mechanisms of neurodegeneration in the entorhinal cortex that underlie its selec-tive vulnerability during the pathogenesis of Alzheimer’s disease. Biol. Open, 2021, 10(1), bio056796.
[18]
Yeung, J.H.Y.; Walby, J.L.; Palpagama, T.H.; Turner, C.; Waldvogel, H.J.; Faull, R.L.M.; Kwakowsky, A. Glutamatergic receptor expres-sion changes in the Alzheimer’s disease hippocampus and entorhinal cortex. Brain Pathol., 2021, 31(6), e13005.
[http://dx.doi.org/10.1111/bpa.13005] [PMID: 34269494]
[19]
Delhaye, E.; Bahri, M.A.; Salmon, E.; Bastin, C. Impaired perceptual integration and memory for unitized representations are associated with perirhinal cortex atrophy in Alzheimer’s disease. Neurobiol. Aging, 2019, 73, 135-144.
[20]
Fogwe, L.A.; Reddy, V.; Mesfin, F.B. Neuroanatomy, Hippocampus. In: StatPearls; StatPearls Publishing: Treasure Island, FL, 2021.
[21]
Dhikav, V.; Anand, K.S. Hippocampus in health and disease: An overview. Ann. Indian Acad. Neurol., 2012, 15(4), 239-246.
[http://dx.doi.org/10.4103/0972-2327.104323] [PMID: 23349586]
[22]
Khalid, M.; Wu, J.M.; Ali, T.; Moustafa, A.A.; Zhu, Q.; Xiong, R. Green model to adapt classical conditioning learning in the hippocam-pus. Neuroscience, 2020, 426, 201-219.
[http://dx.doi.org/10.1016/j.neuroscience.2019.11.021] [PMID: 31812493]
[23]
Jaroudi, W.; Garami, J.; Garrido, S.; Hornberger, M.; Keri, S.; Moustafa, A.A. Factors underlying cognitive decline in old age and Alz-heimer’s disease: Tarticlehe role of the hippocampus. Rev. Neurosci., 2017, 28(7), 705-714.
[http://dx.doi.org/10.1515/revneuro-2016-0086] [PMID: 28422707]
[24]
O’Keefe, J.; Nadel, L. The hippocampus as a cognitive M.01: UK Oxford University Press. Taube, JS, Ranck, JB. Description and quanti-tative analysis. J. Neurosci., 1978, 10, 420-435.
[25]
Eichenbaum, H. The hippocampus as a cognitive map of social space. Neuron, 2015, 87(1), 9-11.
[http://dx.doi.org/10.1016/j.neuron.2015.06.013] [PMID: 26139366]
[26]
Rao, Y.L.; Ganaraja, B.; Murlimanju, B.V.; Joy, T.; Krishnamurthy, A.; Agrawal, A. Hippocampus and its involvement in Alzheimer’s disease: A review. 3 Biotech, 2022, 12(2), 55.
[http://dx.doi.org/10.1007/s13205-022-03123-4] [PMID: 35116217]
[27]
Spoleti, E.; Krashia, P.; La Barbera, L.; Nobili, A.; Lupascu, C.A.; Giacalone, E.; Keller, F.; Migliore, M.; Renzi, M.; D’Amelio, M. Early derailment of firing properties in CA1 pyramidal cells of the ventral hippocampus in an Alzheimer’s disease mouse model. Exp. Neurol., 2022, 350, 113969.
[http://dx.doi.org/10.1016/j.expneurol.2021.113969] [PMID: 34973962]
[28]
Vijayakumar, A.; Vijayakumar, A. Comparison of hippocampal volume in dementia subtypes. ISRN Radiol., 2012, 2013, 174524.
[PMID: 24959551]
[29]
van Hoesen, G.W.; Hyman, B.T.; Damasio, A.R. Entorhinal cortex pathology in Alzheimer’s disease. Hippocampus, 1991, 1(1), 1-8.
[http://dx.doi.org/10.1002/hipo.450010102] [PMID: 1669339]
[30]
Juottonen, K.; Lehtovirta, M.; Helisalmi, S.; Sr, P.J.R.; Soininen, H. Major decrease in the volume of the entorhinal cortex in patients with Alzheimer’s disease carrying the apolipoprotein E epsilon 4 allele. J. Neurol. Neurosurg. Psychiatry, 1998, 65(3), 322-327.
[http://dx.doi.org/10.1136/jnnp.65.3.322] [PMID: 9728943]
[31]
Leandrou, S.; Lamnisos, D.; Mamais, I.; Kyriacou, P.A.; Pattichis, C.S. Alzheimer’s, D. Assessment of Alzheimer’s disease based on texture analysis of the entorhinal cortex. Front. Aging Neurosci., 2020, 12, 176.
[http://dx.doi.org/10.3389/fnagi.2020.00176] [PMID: 32714177]
[32]
Leandrou, S.; Petroudi, S.; Kyriacou, P.A.; Reyes-Aldasoro, C.C.; Pattichis, C.S. Quantitative MRI brain studies in mild cognitive impair-ment and Alzheimer’s Disease: A methodological review. IEEE Rev. Biomed. Eng., 2018, 11, 97-111.
[http://dx.doi.org/10.1109/RBME.2018.2796598] [PMID: 29994606]
[33]
Kulason, S.; Xu, E.; Tward, D.J.; Bakker, A.; Albert, M.; Younes, L.; Miller, M.I. Entorhinal and transentorhinal atrophy in preclinical Alzheimer’s Disease. Front. Neurosci., 2020, 14, 804.
[http://dx.doi.org/10.3389/fnins.2020.00804] [PMID: 32973425]
[34]
Khan, U.A.; Liu, L.; Provenzano, F.A.; Berman, D.E.; Profaci, C.P.; Sloan, R.; Mayeux, R.; Duff, K.E.; Small, S.A. Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer’s disease. Nat. Neurosci., 2014, 17(2), 304-311.
[http://dx.doi.org/10.1038/nn.3606] [PMID: 24362760]
[35]
Fjell, A.M.; McEvoy, L.; Holland, D.; Dale, A.M.; Walhovd, K.B. What is normal in normal aging? Effects of aging, amyloid and Alz-heimer’s disease on the cerebral cortex and the hippocampus. Prog. Neurobiol., 2014, 117, 20-40.
[http://dx.doi.org/10.1016/j.pneurobio.2014.02.004] [PMID: 24548606]
[36]
Kobro-Flatmoen, A.; Lagartos-Donate, M.J.; Aman, Y.; Edison, P.; Witter, M.P.; Fang, E.F. Re-emphasizing early Alzheimer’s disease pathology starting in select entorhinal neurons, with a special focus on mitophagy. Ageing Res. Rev., 2021, 67, 101307.
[http://dx.doi.org/10.1016/j.arr.2021.101307] [PMID: 33621703]
[37]
Chrobak, J.J.; Lörincz, A.; Buzsáki, G. Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus, 2000, 10(4), 457-465.
[http://dx.doi.org/10.1002/1098-1063(2000)10:4<457::AIDHIPO12>3.0.CO;2-Z] [PMID: 10985285]
[38]
Zhang, S.J.; Ye, J.; Couey, J.J.; Witter, M.; Moser, E.I.; Moser, M.B. Functional connectivity of the entorhinal–hippocampal space circuit. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369(1635), 20120516.
[http://dx.doi.org/10.1098/rstb.2012.0516] [PMID: 24366130]
[39]
Devanand, D.P.; Bansal, R.; Liu, J.; Hao, X.; Pradhaban, G.; Peterson, B.S. MRI hippocampal and entorhinal cortex mapping in predicting conversion to Alzheimer’s disease. Neuroimage, 2012, 60(3), 1622-1629.
[http://dx.doi.org/10.1016/j.neuroimage.2012.01.075] [PMID: 22289801]
[40]
Ma, D.; Fetahu, I.S.; Wang, M.; Fang, R.; Li, J.; Liu, H.; Gramyk, T.; Iwanicki, I.; Gu, S.; Xu, W.; Tan, L.; Wu, F.; Shi, Y.G. The fusiform gyrus exhibits an epigenetic signature for Alzheimer’s disease. Clin. Epigenetics, 2020, 12(1), 129.
[http://dx.doi.org/10.1186/s13148-020-00916-3] [PMID: 32854783]
[41]
Friedman, B.A.; Srinivasan, K.; Ayalon, G.; Meilandt, W.J.; Lin, H.; Huntley, M.A.; Cao, Y.; Lee, S.H.; Haddick, P.C.G.; Ngu, H.; Modru-san, Z.; Larson, J.L.; Kaminker, J.S.; van der Brug, M.P.; Hansen, D.V. Diverse brain myeloid expression profiles reveal distinct microgli-al activation states and aspects of Alzheimer’s disease not evident in mouse models. Cell Rep., 2018, 22(3), 832-847.
[http://dx.doi.org/10.1016/j.celrep.2017.12.066] [PMID: 29346778]
[42]
Huang, Y; Mahley, RW polipoprotein E: Structure and function in lipid metabolism, neurobiology, and Alzheimer's diseases. Neurobiol. dis., 2014, 72(Pt A), 3-12.
[43]
Uddin, M.S.; Kabir, M.T.; Al Mamun, A.; Abdel-Daim, M.M.; Barreto, G.E.; Ashraf, G.M. APOE and Alzheimer’s Disease: Evidence mounts that targeting APOE4 may combat Alzheimer’s Pathogenesis. Mol. Neurobiol., 2019, 56(4), 2450-2465.
[http://dx.doi.org/10.1007/s12035-018-1237-z] [PMID: 30032423]
[44]
Mahley, R.W.; Weisgraber, K.H.; Huang, Y. Apolipoprotein E4: A causative factor and therapeutic target in neuropathology, including Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2006, 103(15), 5644-5651.
[http://dx.doi.org/10.1073/pnas.0600549103] [PMID: 16567625]
[45]
Wisniewski, T.; Drummond, E. APOE-amyloid interaction: Therapeutic targets. Neurobiol. Dis., 2020, 138, 104784.
[http://dx.doi.org/10.1016/j.nbd.2020.104784] [PMID: 32027932]
[46]
Montagne, A.; Nikolakopoulou, A.M.; Huuskonen, M.T.; Sagare, A.P.; Lawson, E.J.; Lazic, D.; Rege, S.V.; Grond, A.; Zuniga, E.; Barnes, S.R.; Prince, J.; Sagare, M.; Hsu, C.J.; LaDu, M.J.; Jacobs, R.E.; Zlokovic, B.V. APOE4 accelerates advanced-stage vascular and neuro-degenerative disorder in old Alzheimer’s mice via cyclophilin A independently of amyloid-β. Nature Aging, 2021, 1(6), 506-520.
[http://dx.doi.org/10.1038/s43587-021-00073-z] [PMID: 35291561]
[47]
La Joie, R.; Visani, A.V.; Lesman-Segev, O.H.; Baker, S.L.; Edwards, L.; Iaccarino, L.; Soleimani-Meigooni, D.N.; Mellinger, T.; Janabi, M.; Miller, Z.A.; Perry, D.C.; Pham, J.; Strom, A.; Gorno-Tempini, M.L.; Rosen, H.J.; Miller, B.L.; Jagust, W.J.; Rabinovici, G.D. Associa-tion of APOE4 and clinical variability in Alzheimer disease with the pattern of tau- and amyloid-PET. Neurology, 2021, 96(5), e650-e661.
[http://dx.doi.org/10.1212/WNL.0000000000011270] [PMID: 33262228]
[48]
Konishi, K.; Joober, R.; Poirier, J.; MacDonald, K.; Chakravarty, M.; Patel, R.; Breitner, J.; Bohbot, V.D. Healthy versus entorhinal cortical atrophy identification in asymptomatic apoe4 carriers at risk for Alzheimer’s Disease. J. Alzheimers Dis., 2018, 61(4), 1493-1507.
[http://dx.doi.org/10.3233/JAD-170540] [PMID: 29278888]
[49]
Litvinchuk, A.; Huynh, T.P.V.; Shi, Y.; Jackson, R.J.; Finn, M.B.; Manis, M.; Francis, C.M.; Tran, A.C.; Sullivan, P.M.; Ulrich, J.D.; Hy-man, B.T.; Cole, T.; Holtzman, D.M. Apolipoprotein E4 reduction with antisense oligonucleotides decreases neurodegeneration in a tauopathy model. Ann. Neurol., 2021, 89(5), 952-966.
[http://dx.doi.org/10.1002/ana.26043] [PMID: 33550655]
[50]
Gillespie, A.K.; Jones, E.A.; Lin, Y.H.; Karlsson, M.P.; Kay, K.; Yoon, S.Y.; Tong, L.M.; Nova, P.; Carr, J.S.; Frank, L.M.; Huang, Y. Apolipoprotein E4 causes age-dependent disruption of slow gamma oscillations during hippocampal sharp-wave ripples. Neuron, 2016, 90(4), 740-751.
[http://dx.doi.org/10.1016/j.neuron.2016.04.009] [PMID: 27161522]
[51]
Holcomb, L.; Gordon, M.N.; McGowan, E.; Yu, X.; Benkovic, S.; Jantzen, P.; Wright, K.; Saad, I.; Mueller, R.; Morgan, D.; Sanders, S.; Zehr, C.; O’Campo, K.; Hardy, J.; Prada, C.M.; Eckman, C.; Younkin, S.; Hsiao, K.; Duff, K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med., 1998, 4(1), 97-100.
[http://dx.doi.org/10.1038/nm0198-097] [PMID: 9427614]
[52]
Nagy, Z.S.; Esiri, M.M.; Jobst, K.A.; Johnston, C.; Litchfield, S.; Sim, E.; Smith, A.D. Influence of the apolipoprotein E genotype on amy-loid deposition and neurofibrillary tangle formation in Alzheimer’s disease. Neuroscience, 1995, 69(3), 757-761.
[http://dx.doi.org/10.1016/0306-4522(95)00331-C] [PMID: 8596645]
[53]
Emrani, S.; Arain, H.A.; DeMarshall, C.; Nuriel, T. APOE4 is associated with cognitive and pathological heterogeneity in patients with Alzheimer’s disease: a systematic review. Alzheimers Res. Ther., 2020, 12(1), 141.
[http://dx.doi.org/10.1186/s13195-020-00712-4] [PMID: 33148345]
[54]
Soininen, H.; Kosunen, O.; Helisalmi, S.; Mannermaa, A.; Paljärvi, L.; Talasniemi, S.; Ryynänen, M.; Riekkinen, P. Sr A severe loss of choline acetyltransferase in the frontal cortex of Alzheimer patients carrying apolipoprotein ε4 allele. Neurosci. Lett., 1995, 187(2), 79-82.
[http://dx.doi.org/10.1016/0304-3940(95)11343-6] [PMID: 7783963]
[55]
Buttini, M.; Yu, G.Q.; Shockley, K.; Huang, Y.; Jones, B.; Masliah, E.; Mallory, M.; Yeo, T.; Longo, F.M.; Mucke, L. Modulation of Alz-heimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpres-sion of amyloid beta peptides but not on plaque formation. J. Neurosci., 2002, 22(24), 10539-10548.
[http://dx.doi.org/10.1523/JNEUROSCI.22-24-10539.2002] [PMID: 12486146]
[56]
Dolejší, E.; Liraz, O.; Rudajev, V.; Zimčík, P.; Doležal, V.; Michaelson, D.M. Apolipoprotein E4 reduces evoked hippocampal acetylcho-line release in adult mice. J. Neurochem., 2016, 136(3), 503-509.
[http://dx.doi.org/10.1111/jnc.13417] [PMID: 26526158]
[57]
Giacobini, E.; Pepeu, G. Sex and gender differences in the brain cholinergic system and in the response to therapy of Alzheimer disease with cholinesterase inhibitors. Curr. Alzheimer Res., 2018, 15(11), 1077-1084.
[http://dx.doi.org/10.2174/1567205015666180613111504] [PMID: 29895246]
[58]
Giacobini, E.; Cuello, A.C.; Fisher, A. Reimagining cholinergic therapy for Alzheimer’s disease. Brain, 2022, 145(7), 2250-2275.
[http://dx.doi.org/10.1093/brain/awac096] [PMID: 35289363]
[59]
Tang, X.; Holland, D.; Dale, A.M.; Miller, M.I. APOE affects the volume and shape of the amygdala and the hippocampus in mild cogni-tive impairment and Alzheimer’s Disease: Age matters. J. Alzheimers Dis., 2015, 47(3), 645-660.
[http://dx.doi.org/10.3233/JAD-150262] [PMID: 26401700]
[60]
Hampel, H.; Mesulam, M.M.; Cuello, A.C.; Farlow, M.R.; Giacobini, E.; Grossberg, G.T.; Khachaturian, A.S.; Vergallo, A.; Cavedo, E.; Snyder, P.J.; Khachaturian, Z.S. The cholinergic system in the pathophysiology and treatment of Alzheimer’s disease. Brain, 2018, 141(7), 1917-1933.
[http://dx.doi.org/10.1093/brain/awy132] [PMID: 29850777]
[61]
Wattmo, C.; Wallin, Å.K.; Londos, E.; Minthon, L. Long-term outcome and prediction models of activities of daily living in Alzheimer disease with cholinesterase inhibitor treatment. Alzheimer Dis. Assoc. Disord., 2011, 25(1), 63-72.
[http://dx.doi.org/10.1097/WAD.0b013e3181f5dd97] [PMID: 20847636]
[62]
Wang, R.H.; Bejar, C.; Weinstock, M. Gender differences in the effect of rivastigmine on brain cholinesterase activity and cognitive func-tion in rats. Neuropharmacology, 2000, 39(3), 497-506.
[http://dx.doi.org/10.1016/S0028-3908(99)00157-4] [PMID: 10698015]
[63]
van Beijsterveldt, L.; Geerts, R.; Verhaeghe, T.; Willems, B.; Bode, W.; Lavrijsen, K.; Meuldermans, W. Pharmacokinetics and tissue dis-tribution of galantamine and galantamine-related radioactivity after single intravenous and oral administration in the rat. Arzneimittelforschung, 2004, 54(2), 85-94.
[PMID: 15038457]
[64]
Macgowan, S.H.; Wilcock, G.K.; Scott, M. Effect of gender and apolipoprotein E genotype on response to anticholinesterase therapy in Alzheimer’s disease. Int. J. Geriatr. Psychiatry, 1998, 13(9), 625-630.
[http://dx.doi.org/10.1002/(SICI)1099-1166(199809)13:9<625::AID-GPS835>3.0.CO;2-2] [PMID: 9777427]
[65]
Moustafa, A.A.; Tindle, R.; Alashwal, H.; Diallo, T.M.O. A longitudinal study using latent curve models of groups with mild cognitive impairment and Alzheimer’s disease. J. Neurosci. Methods, 2021, 350, 109040.
[http://dx.doi.org/10.1016/j.jneumeth.2020.109040] [PMID: 33345945]
[66]
Alashwal, H.; Diallo, T.M.O.; Tindle, R.; Moustafa, A.A. Latent class and transition analysis of Alzheimer’s disease data. Front. Comput. Sci., 2020, 2, 551481.
[http://dx.doi.org/10.3389/fcomp.2020.551481]
[67]
Warren, S.L.; Moustafa, A.A.; Alashwal, H. Alzheimer’s Disease Neuroimaging I. Harnessing forgetfulness: Can episodic-memory tests pre-dict early Alzheimer’s disease. Exp. Brain Res., 2021, 239(9), 2925-2937.
[68]
Venugopalan, J.; Tong, L.; Hassanzadeh, H.R.; Wang, M.D. Multimodal deep learning models for early detection of Alzheimer’s disease stage. Sci. Rep., 2021, 11(1), 3254.
[http://dx.doi.org/10.1038/s41598-020-74399-w] [PMID: 33547343]
[69]
Qiu, S.; Joshi, P.S.; Miller, M.I.; Xue, C.; Zhou, X.; Karjadi, C.; Chang, G.H.; Joshi, A.S.; Dwyer, B.; Zhu, S.; Kaku, M.; Zhou, Y.; Aldera-zi, Y.J.; Swaminathan, A.; Kedar, S.; Saint-Hilaire, M.H.; Auerbach, S.H.; Yuan, J.; Sartor, E.A.; Au, R.; Kolachalama, V.B. Development and validation of an interpretable deep learning framework for Alzheimer’s disease classification. Brain, 2020, 143(6), 1920-1933.
[http://dx.doi.org/10.1093/brain/awaa137] [PMID: 32357201]
[70]
Oh, K.; Chung, Y.C.; Kim, K.W.; Kim, W.S.; Oh, I.S. Classification and visualization of Alzheimer’s Disease using volumetric convolu-tional neural network and transfer learning. Sci. Rep., 2019, 9(1), 18150.
[http://dx.doi.org/10.1038/s41598-019-54548-6] [PMID: 31796817]
[71]
El Haj, M.; Moustafa, A.A. Alzheimer’s disease in the pupil: Pupillometry as a biomarker of cognitive processing in Alzheimer’s disease. Alzheimer’s Disease: Understanding Biomarkers, Big Data. Therapy, 2022, 77-85.
[72]
El Haj, M.; Moustafa, A.A.; Gallouj, K.; Robin, F. Visual imagery: The past and future as seen by patients with Alzheimer’s disease. Conscious. Cogn., 2019, 68, 12-22.
[http://dx.doi.org/10.1016/j.concog.2018.12.003] [PMID: 30593998]
[73]
Pike, C.J. Sex and the development of Alzheimer’s disease. J. Neurosci. Res., 2017, 95(1-2), 671-680.
[http://dx.doi.org/10.1002/jnr.23827] [PMID: 27870425]
[74]
Hauser, P.S.; Narayanaswami, V.; Ryan, R.O.; Apolipoprotein, E.; Apolipoprotein, E. From lipid transport to neurobiology. Prog. Lipid Res., 2011, 50(1), 62-74.
[http://dx.doi.org/10.1016/j.plipres.2010.09.001] [PMID: 20854843]
[75]
Nuriel, T.; Angulo, S.L.; Khan, U.; Ashok, A.; Chen, Q.; Figueroa, H.Y.; Emrani, S.; Liu, L.; Herman, M.; Barrett, G.; Savage, V.; Buitrago, L.; Cepeda-Prado, E.; Fung, C.; Goldberg, E.; Gross, S.S.; Hussaini, S.A.; Moreno, H.; Small, S.A.; Duff, K.E. Neuronal hyperactivity due to loss of inhibitory tone in APOE4 mice lacking Alzheimer’s disease-like pathology. Nat. Commun., 2017, 8(1), 1464.
[http://dx.doi.org/10.1038/s41467-017-01444-0] [PMID: 29133888]
[76]
Sohn, H.Y.; Kim, S.I.; Park, J.Y.; Park, S.H.; Koh, Y.H.; Kim, J.; Jo, C. ApoE4 attenuates autophagy via FoxO3a repression in the brain. Sci. Rep., 2021, 11(1), 17604.
[http://dx.doi.org/10.1038/s41598-021-97117-6] [PMID: 34475505]
[77]
Moon, W.J.; Lim, C.; Ha, I.H.; Kim, Y.; Moon, Y.; Kim, H.J.; Han, S.H. Hippocampal blood–brain barrier permeability is related to the APOE4 mutation status of elderly individuals without dementia. J. Cereb. Blood Flow Metab., 2021, 41(6), 1351-1361.
[http://dx.doi.org/10.1177/0271678X20952012] [PMID: 32936729]
[78]
Régy, M.; Dugravot, A.; Sabia, S.; Fayosse, A.; Mangin, J.F.; Chupin, M.; Fischer, C.; Bouteloup, V.; Dufouil, C.; Chêne, G.; Paquet, C.; Hanseeuw, B.; Singh-Manoux, A.; Dumurgier, J. Association of APOE ε4 with cerebral gray matter volumes in non-demented older adults: The MEMENTO cohort study. Neuroimage, 2022, 250, 118966.
[http://dx.doi.org/10.1016/j.neuroimage.2022.118966] [PMID: 35122970]
[79]
Du, A.T.; Schuff, N.; Kramer, J.H.; Ganzer, S.; Zhu, X.P.; Jagust, W.J.; Miller, B.L.; Reed, B.R.; Mungas, D.; Yaffe, K.; Chui, H.C.; Weiner, M.W. Higher atrophy rate of entorhinal cortex than hippocampus in AD. Neurology, 2004, 62(3), 422-427.
[http://dx.doi.org/10.1212/01.WNL.0000106462.72282.90] [PMID: 14872024]
[80]
Du, A.T.; Schuff, N.; Amend, D.; Laakso, M.P.; Hsu, Y.Y.; Jagust, W.J.; Yaffe, K.; Kramer, J.H.; Reed, B.; Norman, D.; Chui, H.C.; Weiner, M.W. Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer’s dis-ease. J. Neurol. Neurosurg. Psychiatry, 2001, 71(4), 441-447.
[http://dx.doi.org/10.1136/jnnp.71.4.441] [PMID: 11561025]
[81]
Varon, D.; Loewenstein, D.A.; Potter, E.; Greig, M.T.; Agron, J.; Shen, Q.; Zhao, W.; Celeste Ramirez, M.; Santos, I.; Barker, W.; Potter, H.; Duara, R. Minimal atrophy of the entorhinal cortex and hippocampus: Progression of cognitive impairment. Dement. Geriatr. Cogn. Disord., 2011, 31(4), 276-283.
[http://dx.doi.org/10.1159/000324711] [PMID: 21494034]
[82]
Zhou, M.; Zhang, F.; Zhao, L.; Qian, J.; Dong, C. Entorhinal cortex: A good biomarker of mild cognitive impairment and mild Alzheimer’s disease. Rev. Neurosci., 2016, 27(2), 185-195.
[http://dx.doi.org/10.1515/revneuro-2015-0019] [PMID: 26444348]
[83]
Mecca, A.P.; Chen, M.K.; O’Dell, R.S.; Naganawa, M.; Toyonaga, T.; Godek, T.A.; Harris, J.E.; Bartlett, H.H.; Zhao, W.; Banks, E.R.; Ni, G.S.; Rogers, K.; Gallezot, J.D.; Ropchan, J.; Emery, P.R.; Nabulsi, N.B.; Vander Wyk, B.C.; Arnsten, A.F.T.; Huang, Y.; Carson, R.E.; van Dyck, C.H. Association of entorhinal cortical tau deposition and hippocampal synaptic density in older individuals with normal cognition and early Alzheimer’s disease. Neurobiol. Aging, 2022, 111, 44-53.
[http://dx.doi.org/10.1016/j.neurobiolaging.2021.11.004] [PMID: 34963063]
[84]
Shaw, P.; Lerch, J.P.; Pruessner, J.C.; Taylor, K.N.; Rose, A.B.; Greenstein, D.; Clasen, L.; Evans, A.; Rapoport, J.L.; Giedd, J.N. Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study. Lancet Neurol., 2007, 6(6), 494-500.
[http://dx.doi.org/10.1016/S1474-4422(07)70106-0] [PMID: 17509484]
[85]
Lehtovirta, M.; Laakso, M.P.; Soininen, H.; Helisalmi, S.; Mannermaa, A.; Helkala, E.L.; Partanen, K.; Ryynänen, M.; Vainio, P.; Hartikainen, P.; Riekkinen, P.J., Sr Volumes of hippocampus, amygdala and frontal lobe in Alzheimer patients with different apolipopro-tein E genotypes. Neuroscience, 1995, 67(1), 65-72.
[http://dx.doi.org/10.1016/0306-4522(95)00014-A] [PMID: 7477910]
[86]
Hsu, M.; Dedhia, M.; Crusio, W.E. Delprato, A Sex differences in gene expression patterns associated with the APOE4 allele. F1000 Res., 2019, 8, 387.
[87]
Li, X.; Zhou, S.; Zhu, W.; Li, X.; Gao, Z.; Li, M.; Luo, S.; Wu, X.; Tian, Y.; Yu, Y. Sex difference in network topology and education correlated with sex difference in cognition during the disease process of Alzheimer. Front. Aging Neurosci., 2021, 13, 639529.
[http://dx.doi.org/10.3389/fnagi.2021.639529] [PMID: 34149392]
[88]
Wang, Z.T.; Li, K.Y.; Tan, C.C.; Xu, W.; Shen, X.N.; Cao, X.P.; Wang, P.; Bi, Y.L.; Dong, Q.; Tan, L.; Yu, J.T. Associations of alcohol consumption with cerebrospinal fluid biomarkers of Alzheimer’s disease pathology in cognitively intact older adults: The CABLE Study. J. Alzheimers Dis., 2021, 82(3), 1045-1054.
[http://dx.doi.org/10.3233/JAD-210140] [PMID: 34151793]
[89]
Linnemann, C.; Lang, U.E. Pathways connecting late-life depression and dementia. Front. Pharmacol., 2020, 11, 279.
[http://dx.doi.org/10.3389/fphar.2020.00279] [PMID: 32231570]
[90]
Nebel, R.A.; Aggarwal, N.T.; Barnes, L.L.; Gallagher, A.; Goldstein, J.M.; Kantarci, K.; Mallampalli, M.P.; Mormino, E.C.; Scott, L.; Yu, W.H.; Maki, P.M.; Mielke, M.M. Understanding the impact of sex and gender in Alzheimer’s disease: A call to action. Alzheimers Dement., 2018, 14(9), 1171-1183.
[http://dx.doi.org/10.1016/j.jalz.2018.04.008] [PMID: 29907423]
[91]
Ferretti, M.T.; Iulita, M.F.; Cavedo, E.; Chiesa, P.A.; Schumacher Dimech, A.; Santuccione Chadha, A.; Baracchi, F.; Girouard, H.; Misoch, S.; Giacobini, E.; Depypere, H.; Hampel, H. Sex differences in Alzheimer disease-the gateway to precision medicine. Nat. Rev. Neurol., 2018, 14(8), 457-469.
[http://dx.doi.org/10.1038/s41582-018-0032-9] [PMID: 29985474]
[92]
Farrer, L.A.; Cupples, L.A.; Haines, J.L.; Hyman, B.; Kukull, W.A.; Mayeux, R.; Myers, R.H.; Pericak-Vance, M.A.; Risch, N.; van Duijn, C.M. Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. JAMA, 1997, 278(16), 1349-1356.
[http://dx.doi.org/10.1001/jama.1997.03550160069041] [PMID: 9343467]
[93]
Shen, S.; Zhou, W.; Chen, X.; Zhang, J. Sex differences in the association ofAPOE ε4 genotype with longitudinal hippocampal atrophy in cognitively normal older people. Eur. J. Neurol., 2019, 26(11), 1362-1369.
[http://dx.doi.org/10.1111/ene.13987] [PMID: 31102429]
[94]
Wang, X.; Zhou, W.; Ye, T.; Lin, X.; Zhang, J. Sex Difference in the association of APOE4 with memory decline in mild cognitive impair-ment. J. Alzheimers Dis., 2019, 69(4), 1161-1169.
[http://dx.doi.org/10.3233/JAD-181234] [PMID: 31127771]
[95]
Andrew, M.K.; Tierney, M.C. The puzzle of sex, gender and Alzheimer’s disease: Why are women more often affected than men? Womens Health, 2018, 14.
[http://dx.doi.org/10.1177/1745506518817995]
[96]
Podcasy, J.L.; Epperson, C.N. Considering sex and gender in Alzheimer disease and other dementias. Dialogues Clin. Neurosci., 2022, 18(4), 437-446.
[PMID: 28179815]
[97]
Subramaniapillai, S.; Almey, A.; Natasha Rajah, M.; Einstein, G. Sex and gender differences in cognitive and brain reserve: Implications for Alzheimer’s disease in women. Front. Neuroendocrinol., 2021, 60, 100879.
[http://dx.doi.org/10.1016/j.yfrne.2020.100879] [PMID: 33137359]
[98]
Rahman, A.; Jackson, H.; Hristov, H.; Isaacson, R.S.; Saif, N.; Shetty, T.; Etingin, O.; Henchcliffe, C.; Brinton, R.D.; Mosconi, L. Sex and gender driven modifiers of Alzheimer’s: The role for estrogenic control across age, race, medical, and lifestyle risks. Front. Aging Neurosci., 2019, 11, 315.
[http://dx.doi.org/10.3389/fnagi.2019.00315] [PMID: 31803046]
[99]
Russell-Williams, J.; Jaroudi, W.; Perich, T.; Hoscheidt, S.; El Haj, M.; Moustafa, A.A. Mindfulness and meditation: Treating cognitive impairment and reducing stress in dementia. Rev. Neurosci., 2018, 29(7), 791-804.
[http://dx.doi.org/10.1515/revneuro-2017-0066] [PMID: 29466242]
[100]
Filon, J.R.; Intorcia, A.J.; Sue, L.I.; Vazquez Arreola, E.; Wilson, J.; Davis, K.J.; Sabbagh, M.N.; Belden, C.M.; Caselli, R.J.; Adler, C.H.; Woodruff, B.K.; Rapscak, S.Z.; Ahern, G.L.; Burke, A.D.; Jacobson, S.; Shill, H.A.; Driver-Dunckley, E.; Chen, K.; Reiman, E.M.; Beach, T.G.; Serrano, G.E. Gender Differences in Alzheimer Disease: Brain atrophy, histopathology burden, and cognition. J. Neuropathol. Exp. Neurol., 2016, 75(8), 748-754.
[http://dx.doi.org/10.1093/jnen/nlw047] [PMID: 27297671]
[101]
Sampedro, F.; Vilaplana, E.; de Leon, M.J.; Alcolea, D.; Pegueroles, J.; Montal, V.; Carmona-Iragui, M.; Sala, I.; Sánchez-Saudinos, M.B.; Antón-Aguirre, S.; Morenas-Rodríguez, E.; Camacho, V.; Falcón, C.; Pavía, J.; Ros, D.; Clarimón, J.; Blesa, R.; Lleó, A.; Fortea, J. APOE -by-sex interactions on brain structure and metabolism in healthy elderly controls. Oncotarget, 2015, 6(29), 26663-26674.
[http://dx.doi.org/10.18632/oncotarget.5185] [PMID: 26397226]
[102]
Barrett-Connor, E.; Kritz-Silverstein, D. Estrogen replacement therapy and cognitive function in older women. JAMA, 1993, 269(20), 2637-2641.
[http://dx.doi.org/10.1001/jama.1993.03500200051032] [PMID: 8487446]
[103]
Reilly, S.L.; Ferrell, R.E.; Sing, C.F. The gender-specific apolipoprotein E genotype influence on the distribution of plasma lipids and apolipoproteins in the population of Rochester, MN. III. Correlations and covariances. Am. J. Hum. Genet., 1994, 55(5), 1001-1018.
[PMID: 7977338]
[104]
Sundermann, E.E.; Maki, P.M.; Reddy, S.; Bondi, M.W.; Biegon, A. Women’s higher brain metabolic rate compensates for early Alz-heimer’s pathology. Alzheimers Dement., 2020, 12(1), e12121.
[http://dx.doi.org/10.1002/dad2.12121] [PMID: 33251322]
[105]
Sundermann, E.E.; Maki, P.M.; Rubin, L.H.; Lipton, R.B.; Landau, S.; Biegon, A. Female advantage in verbal memory. Neurology, 2016, 87(18), 1916-1924.
[http://dx.doi.org/10.1212/WNL.0000000000003288] [PMID: 27708128]
[106]
Sundermann, E.E.; Biegon, A.; Rubin, L.H.; Lipton, R.B.; Mowrey, W.; Landau, S.; Maki, P.M. Better verbal memory in women than men in MCI despite similar levels of hippocampal atrophy. Neurology, 2016, 86(15), 1368-1376.
[http://dx.doi.org/10.1212/WNL.0000000000002570] [PMID: 26984945]
[107]
Sundermann, E.E.; Biegon, A.; Rubin, L.H.; Lipton, R.B.; Landau, S.; Maki, P.M. Does the female advantage in verbal memory contribute to underestimating Alzheimer’s disease pathology in women versus men? J. Alzheimers Dis., 2017, 56(3), 947-957.
[http://dx.doi.org/10.3233/JAD-160716] [PMID: 28106548]
[108]
Edland, S.D.; Rocca, W.A.; Petersen, R.C.; Cha, R.H.; Kokmen, E. Dementia and Alzheimer disease incidence rates do not vary by sex in Rochester, Minn. Arch. Neurol., 2002, 59(10), 1589-1593.
[http://dx.doi.org/10.1001/archneur.59.10.1589] [PMID: 12374497]
[109]
Wolff, J.R.; Missler, M. Synaptic remodelling and elimination as integral processes of synaptogenesis. APMIS, 1993(Suppl. 40), 9-23.
[110]
Faghihi, F.; Alashwal, H.; Moustafa, A.A. A synaptic pruning-based spiking neural network for hand-written digits classification. Front. Artif. Intell., 2022, 5, 680165.
[http://dx.doi.org/10.3389/frai.2022.680165] [PMID: 35280233]
[111]
Brucato, F.H.; Benjamin, D.E. Synaptic pruning in Alzheimer’s disease: Role of the complement system. Glob. J. Med. Res., 2020, 20(6), 1-20.
[http://dx.doi.org/10.34257/GJMRFVOL20IS6PG1] [PMID: 32982106]
[112]
Masliah, E.; Crews, L.; Hansen, L. Synaptic remodeling during aging and in Alzheimer’s disease. J. Alzheimers Dis., 2006, 9(s3), 91-99.
[http://dx.doi.org/10.3233/JAD-2006-9S311] [PMID: 16914848]
[113]
Hong, S.; Beja-Glasser, V.F.; Nfonoyim, B.M.; Frouin, A.; Li, S.; Ramakrishnan, S. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science, 2016, 352(6286), 712-716.
[http://dx.doi.org/10.1126/science.aad8373]
[114]
Ghebremedhin, E.; Schultz, C.; Braak, E.; Braak, H. High frequency of apolipoprotein E epsilon4 allele in young individuals with very mild Alzheimer’s disease-related neurofibrillary changes. Exp. Neurol., 1998, 153(1), 152-155.
[http://dx.doi.org/10.1006/exnr.1998.6860] [PMID: 9743577]
[115]
Haier, R.J.; Alkire, M.T.; White, N.S.; Uncapher, M.R.; Head, E.; Lott, I.T.; Cotman, C.W. Temporal cortex hypermetabolism in Down syndrome prior to the onset of dementia. Neurology, 2003, 61(12), 1673-1679.
[http://dx.doi.org/10.1212/01.WNL.0000098935.36984.25] [PMID: 14694028]
[116]
DiBattista, A.M.; Dumanis, S.B.; Newman, J.; Rebeck, G.W. Identification and modification of amyloid-independent phenotypes of AP-OE4 mice. Exp. Neurol., 2016, 280, 97-105.
[http://dx.doi.org/10.1016/j.expneurol.2016.04.014] [PMID: 27085394]
[117]
Obenhaus, H.A.; Zong, W.; Jacobsen, R.I.; Rose, T.; Donato, F.; Chen, L.; Cheng, H.; Bonhoeffer, T.; Moser, M.B.; Moser, E.I. Functional network topography of the medial entorhinal cortex. Proc. Natl. Acad. Sci., 2022, 119(7), e2121655119.
[http://dx.doi.org/10.1073/pnas.2121655119] [PMID: 35135885]
[118]
Tukker, J.J.; Beed, P.; Brecht, M.; Kempter, R.; Moser, E.I.; Schmitz, D. Microcircuits for spatial coding in the medial entorhinal cortex. Physiol. Rev., 2022, 102(2), 653-688.
[http://dx.doi.org/10.1152/physrev.00042.2020] [PMID: 34254836]
[119]
Kunz, L.; Schroder, T.N.; Lee, H.; Montag, C.; Lachmann, B.; Sariyska, R. Reduced grid-cell-like representations in adults at genetic risk for Alzheimer’s disease. Science, 2015, 350(6259), 430-433.
[http://dx.doi.org/10.1126/science.aac8128]
[120]
Faghihi, F.; Moustafa, A.A. A computational model of pattern separation efficiency in the dentate gyrus with implications in schizophre-nia. Front. Syst. Neurosci., 2015, 9, 42.
[http://dx.doi.org/10.3389/fnsys.2015.00042] [PMID: 25859189]
[121]
Moustafa, A.A.; Wufong, E.; Servatius, R.J.; Pang, K.C.H.; Gluck, M.A.; Myers, C.E. Why trace and delay conditioning are sometimes (but not always) hippocampal dependent: A computational model. Brain Res., 2013, 1493, 48-67.
[http://dx.doi.org/10.1016/j.brainres.2012.11.020] [PMID: 23178699]
[122]
Moustafa, A.A.; Gluck, M.A. Computational cognitive models of prefrontal-striatal-hippocampal interactions in Parkinson’s disease and schizophrenia. Neural Netw., 2011, 24(6), 575-591.
[http://dx.doi.org/10.1016/j.neunet.2011.02.006] [PMID: 21411277]
[123]
Khalid, M.; Wu, J.; Ali, T.M.; Ameen, T.; Altaher, A.S.; Moustafa, A.A.; Zhu, Q.; Xiong, R. Cortico-Hippocampal computational modeling using quantum-inspired neural networks. Front. Comput. Neurosci., 2020, 14, 80.
[http://dx.doi.org/10.3389/fncom.2020.00080] [PMID: 33224031]

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