Animal models in neuroscience with alternative approaches: Evolutionary, biomedical, and ethical perspectives

Sabina Neziri , Ahmet Efe Köseoğlu , Gülsüm Deniz Köseoğlu , Buminhan Özgültekin , Nehir Özdemir Özgentürk

Animal Models and Experimental Medicine ›› 2024, Vol. 7 ›› Issue (6) : 868 -880.

PDF (1860KB)
Animal Models and Experimental Medicine ›› 2024, Vol. 7 ›› Issue (6) : 868 -880. DOI: 10.1002/ame2.12487
REVIEW

Animal models in neuroscience with alternative approaches: Evolutionary, biomedical, and ethical perspectives

Author information +
History +
PDF (1860KB)

Abstract

Animal models have been a crucial tool in neuroscience research for decades, providing insights into the biomedical and evolutionary mechanisms of the nervous system, disease, and behavior. However, their use has raised concerns on several ethical, clinical, and scientific considerations. The welfare of animals and the 3R principles (replacement, reduction, refinement) are the focus of the ethical concerns, targeting the importance of reducing the stress and suffering of these models. Several laws and guidelines are applied and developed to protect animal rights during experimenting. Concurrently, in the clinic and biomedical fields, discussions on the relevance of animal model findings on human organisms have increased. Latest data suggest that in a considerable amount of time the animal model results are not translatable in humans, costing time and money. Alternative methods, such as in vitro (cell culture, microscopy, organoids, and micro physiological systems) techniques and in silico (computational) modeling, have emerged as potential replacements for animal models, providing more accurate data in a minimized cost. By adopting alternative methods and promoting ethical considerations in research practices, we can achieve the 3R goals while upholding our responsibility to both humans and other animals. Our goal is to present a thorough review of animal models used in neuroscience from the biomedical, evolutionary, and ethical perspectives. The novelty of this research lies in integrating diverse points of views to provide an understanding of the advantages and disadvantages of animal models in neuroscience and in discussing potential alternative methods.

Keywords

alternatives / animal models / biomedicine / ethics / evolution / neuroscience

Cite this article

Download citation ▾
Sabina Neziri, Ahmet Efe Köseoğlu, Gülsüm Deniz Köseoğlu, Buminhan Özgültekin, Nehir Özdemir Özgentürk. Animal models in neuroscience with alternative approaches: Evolutionary, biomedical, and ethical perspectives. Animal Models and Experimental Medicine, 2024, 7(6): 868-880 DOI:10.1002/ame2.12487

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Neuroscience. Collection Development Guidelines of the National Library of Medicine. National Library of Medicine (U.S.); 2003. https://www.ncbi.nlm.nih.gov/books/NBK518776/

[2]

Romanova EV, Sweedler JV. Animal model systems in neuroscience. ACS Chem Neurosci. 2018;9(8):1869-1870.

[3]

Sandrone S. The amazing history of neuroscience. Frontiers for Young Minds; 2023.

[4]

Ericsson AC, Crim MJ, Franklin CL. A brief history of animal modeling. Mo Med. 2013;110(3):201-205.

[5]

Piccolino M, Bresadola M. Shocking Frogs: Galvani, Volta, and the Electric Origins of Neuroscience. Oxford University Press; 2013.

[6]

Wilson-Sanders SE. Invertebrate models for biomedical research, testing, and education. ILAR J. 2011;52(2):126-152.

[7]

Hickman DL, Johnson J, Vemulapalli TH, Crisler JR, Shepherd R. Commonly used animal models. Principles of Animal Research for Graduate and Undergraduate Students; Elsevier; 2017:117-175.

[8]

Baxter VK, Griffin DE. Animal models. Viral Pathog (Third edition) 2016;125-138.

[9]

Chesselet M-F, Carmichael ST. Animal models of neurological disorders. Neurotherapeutics. 2012;9(2):241-244.

[10]

Arenas Gómez CM, Echeverri K. Salamanders: the molecular basis of tissue regeneration and its relevance to human disease. Curr Top Dev Biol. 2021;145:235-275.

[11]

Kalueff AV, Stewart AM, Gerlai R. Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol Sci. 2014;35(2):63-75.

[12]

Moroz LL. Aplysia. Curr Biol. 2011;21(2):R60-R61.

[13]

Setia H, Muotri AR. Brain organoids as a model system for human neurodevelopment and disease. Semin Cell Dev Biol. 2019;95:93-97.

[14]

Moon C. New insights into and emerging roles of animal models for neurological disorders. Int J Mol Sci. 2022;23(9):4957.

[15]

Jucker M. The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med. 2010;16(11):1210-1214.

[16]

Mukherjee P, Roy S, Ghosh D, Nandi SK. Role of animal models in biomedical research: a review. Lab Anim Res. 2022;38:18.

[17]

de Sousa AA, Rigby Dames BA, Graff EC, Mohamedelhassan R, Vassilopoulos T, Charvet CJ. Going beyond established model systems of Alzheimer’s disease: companion animals provide novel insights into the neurobiology of aging. Commun Biol. 2023;6(1):655.

[18]

Lowenstine LJ, McManamon R, Terio KA. Comparative pathology of aging great apes: bonobos, chimpanzees, gorillas, and orangutans. Vet Pathol. 2016;53(2):250-276.

[19]

Pollen AA, Kilik U, Lowe CB, Camp JG. Human-specific genetics: new tools to explore the molecular and cellular basis of human evolution. Nat Rev Genet. 2023;24:1-25.

[20]

Grogan KE, Perry GH. Studying human and nonhuman primate evolutionary biology with powerful in vitro and in vivo functional genomics tools. Evol Anthropol Issues News Rev. 2020;29(3):143-158.

[21]

Bechler ME, Byrne L. CNS myelin sheath lengths are an intrinsic property of oligodendrocytes. Curr Biol. 2015;25(18):2411-2416.

[22]

DeLong MR, Benabid A-L. Discovery of high-frequency deep brain stimulation for treatment of Parkinson disease:2014 Lasker award. JAMA. 2014;312(11):1093-1094.

[23]

Rizzolatti G, Fadiga L, Fogassi L, Gallese V. 14 from mirror neurons to imitation: facts and speculations. Imitative Mind Dev Evol Brain Bases. 2002;6:247-266.

[24]

Caggiano V, Fogassi L, Rizzolatti G, Thier P, Casile A. Mirror neurons differentially encode the peripersonal and extrapersonal space of monkeys. Science. 2009;324(5925):403-406.

[25]

Calapai A, Berger M, Niessing M, et al. A cage-based training, cognitive testing and enrichment system optimized for rhesus macaques in neuroscience research. Behav Res Methods. 2017;49:35-45.

[26]

Shi L, Luo X, Jiang J, et al. Transgenic rhesus monkeys carrying the human MCPH1 gene copies show human-like neoteny of brain development. Natl Sci Rev. 2019;6(3):480-493.

[27]

Yang S-H, Cheng P-H, Banta H, et al. Towards a transgenic model of Huntington’s disease in a non-human primate. Nature. 2008;453(7197):7197-7924.

[28]

Krubitzer L. In search of a unifying theory of complex brain evolution. Ann N Y Acad Sci. 2009;1156:44-67.

[29]

Capitanio JP, Emborg ME. Contributions of non-human primates to neuroscience research. Lancet. 2008;371(9618):1126-1135.

[30]

Barlow HB. David Hubel and Torsten Wiesel: their contributions towards understanding the primary visual cortex. Trends Neurosci. 1982;5:145-152.

[31]

Coors ME, Glover JJ, Juengst ET, Sikela JM. The ethics of using transgenic non-human primates to study what makes us human. Nat Rev Genet. 2010;11(9):658-662.

[32]

Chen C, Kim W-Y, Jiang P. Humanized neuronal chimeric mouse brain generated by neonatally engrafted human iPSC-derived primitive neural progenitor cells. JCI Insight. 2016;1(19):e88632.

[33]

Żakowski W. Animal use in neurobiological research. Neuroscience. 2020;433:1-10.

[34]

Francis C, Natarajan S, Lee MT, et al. Divergence of RNA localization between rat and mouse neurons reveals the potential for rapid brain evolution. BMC Genomics. 2014;15(1):1-18.

[35]

Fahey JR, Katoh H, Malcolm R, Perez AV. The case for genetic monitoring of mice and rats used in biomedical research. Mamm Genome. 2013;24(3):89-94.

[36]

Windrem MS, Schanz SJ, Guo M, et al. Neonatal chimerization with human glial progenitor cells can both remyelinate and rescue the otherwise lethally hypomyelinated shiverer mouse. Cell Stem Cell. 2008;2(6):553-565.

[37]

Osipovitch M, Asenjo Martinez A, Mariani JN, et al. Human ESC-derived chimeric mouse models of Huntington’s disease reveal cell-intrinsic defects in glial progenitor cell differentiation. Cell Stem Cell. 2019;24(1):107-122.e7.

[38]

McQuade A, Kang YJ, Hasselmann J, et al. Gene expression and functional deficits underlie TREM2-knockout microglia responses in human models of Alzheimer’s disease. Nat Commun. 2020;11:5370.

[39]

Jin M, Xu R, Wang L, et al. Type-iinterferon signaling drives microglial dysfunction and senescence in human iPSC models of down syndrome and Alzheimer’s disease. Cell Stem Cell. 2022;29(7):1135-1153.e8.

[40]

Juriloff DM, Harris MJ. Insights into the etiology of mammalian neural tube closure defects from developmental, genetic and evolutionary studies. J Dev Biol. 2018;6(3):22.

[41]

de Almeida da Anunciação AR, Favaron PO, de Morais-Pinto L, et al. Central nervous system development in rabbits (Oryctolagus cuniculus L. 1758). Anat Rec. 2021;304(6):1313-1328.

[42]

Davidson JS, West RL, Kotikalapudi P, Maroun LE. Sequence and methylation in the beta/A4 region of the rabbit amyloid precursor protein gene. Biochem Biophys Res Commun. 1992;188(2):905-911.

[43]

Bitel CL, Kasinathan C, Kaswala RH, Klein WL, Frederikse PH. Amyloidβ and tau pathology of Alzheimer’s disease induced by diabetes in a rabbit animal model. J Alzheimers Dis. 2012;32(2):291-305.

[44]

White KA, Swier VJ, Cain JT, et al. A porcine model of neurofibromatosis type 1 that mimics the human disease. JCI Insight. 2018;3(12):e120402.

[45]

Yan S, Tu Z, Liu Z, et al. A huntingtin knockin pig model recapitulates features of selective neurodegeneration in Huntington’s disease. Cell. 2018;173(4):989-1002.

[46]

Partridge B, Rossmeisl JH Jr. Companion animal models of neurological disease. J Neurosci Methods. 2020;331:108484.

[47]

Rabotti GF, Grove AS, Sellers RL, Anderson WR. Induction of multiple brain tumours (gliomata and leptomeningeal sarcomata) in dogs by Rous sarcoma virus. Nature. 1966;209(5026):884-886.

[48]

Ziv L, Muto A, Schoonheim PJ, et al. An affective disorder in zebrafish with mutation of the glucocorticoid receptor. Mol Psychiatry. 2013;18(6):681-691.

[49]

Chakravarty S, Reddy BR, Sudhakar SR, et al. Chronic unpredictable stress (CUS)-induced anxiety and related mood disorders in a zebrafish model: altered brain proteome profile implicates mitochondrial dysfunction. PLoS ONE. 2013;8(5):e63302.

[50]

Sakai C, Ijaz S, Hoffman EJ. Zebrafish models of neurodevelopmental disorders: past, present, and future. Front Mol Neurosci. 2018;11:294.

[51]

Guo S. Using zebrafish to assess the impact of drugs on neural development and function. Expert Opin Drug Discov. 2009;4(7):715-726.

[52]

Benito-Gutiérrez È. A gene catalogue of the amphioxus nervous system. Int J Biol Sci. 2006;2(3):149-160.

[53]

Holland LZ. Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat Rev Neurosci. 2009;10(10):736-746.

[54]

Holland LZ, Carvalho JE, Escriva H, et al. Evolution of bilaterian central nervous systems: a single origin? EvoDevo. 2013;4(1):27.

[55]

Somorjai IML, Somorjai RL, Garcia-Fernàndez J, Escrivà H. Vertebrate-like regeneration in the invertebrate chordate amphioxus. Proc Natl Acad Sci USA. 2012;109(2):517-522.

[56]

Jeibmann A, Paulus W. Drosophila melanogaster as a model organism of brain diseases. Int J Mol Sci. 2009;10(2):407-440.

[57]

Rubin GM, Lewis EB. A brief history of Drosophila’s contributions to genome research. Science (New York, NY). 2000;287(5461):2216-2218.

[58]

Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA. 1996;93(22):12593-12598.

[59]

Mahoney TR, Luo S, Nonet ML. Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay. Nat Protoc. 2006;1(4):1772-1777.

[60]

Sengupta P, Samuel ADT. C. elegans: a model system for systems neuroscience. Curr Opin Neurobiol. 2009;19(6):637-643.

[61]

Calahorro F, Ruiz-Rubio M. Caenorhabditis elegans as an experimental tool for the study of complex neurological diseases: Parkinson’s disease, Alzheimer’s disease and autism spectrum disorder. Invertebr Neurosci. 2011;11(2):73-83.

[62]

Lindsay TH, Thiele TR, Lockery SR. Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans. Nat Commun. 2011;2(1):1304.

[63]

Alexander AG, Marfil V, Li C. Use of Caenorhabditis elegans as a model to study Alzheimer’s disease and other neurodegenerative diseases. Front Genet. 2014;5:279.

[64]

Rapti G. A perspective on C. elegans neurodevelopment: from early visionaries to a booming neuroscience research. J Neurogenet. 2020;34(3–4):259-272.

[65]

Naranjo-Galindo FJ, Ai R, Fang EF, Nilsen HL, SenGupta T. C. elegans as an animal model to study the intersection of DNA repair, aging and neurodegeneration. Front Aging. 2022;3:916118.

[66]

Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science. 2001;294(5544):1030-1038.

[67]

Robertson M, Walter G. Eric Kandel and Aplysia californica: their role in the elucidation of mechanisms of memory and the study of psychotherapy. Acta Neuropsychiatr. 2010;22(4):195-196.

[68]

Kron NS, Fieber LA. Aplysia neurons as a model of Alzheimer’s disease: shared genes and differential expression. J Mol Neurosci. 2022;72(2):287-302.

[69]

Kiani AK, Pheby D, Henehan G, et al. Ethical considerations regarding animal experimentation. J Prev Med Hyg. 2022;63(suppl. 3):E255-E266.

[70]

Morton DB. A model framework for the estimation of animal ‘suffering’: its use in predicting and retrospectively assessing the impact of experiments on animals. Animals. 2023;13(5):800.

[71]

Vashishat A, Patel P, Das Gupta G, Das Kurmi B. Alternatives of animal models for biomedical research: a comprehensive review of modern approaches. Stem Cell Rev Rep. 2024;20(4):881-899.

[72]

Sun D, Gao W, Hu H, Zhou S. Why 90% of clinical drug development fails and how to improve it? Acta Pharm Sin B. 2022;12(7):3049-3062.

[73]

Van Norman GA. Limitations of animal studies for predicting toxicity in clinical trials. JACC Basic Transl Sci. 2019;4(7):845-854.

[74]

Garner JP. The significance of meaning: why do over 90% of behavioral neuroscience results fail to translate to humans, and what can we do to fix it? ILAR J. 2014;55(3):438-456.

[75]

Ransohoff RM. All (animal) models (of neurodegeneration) are wrong. Are they also useful? J Exp Med. 2018;215(12):2955-2958.

[76]

Dawson TM, Golde TE, Lagier-Tourenne C. Animal models of neurodegenerative diseases. Nat Neurosci. 2018;21(10):1370-1379.

[77]

Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods. 2005;2(8):599-605.

[78]

Park J, Koito H, Li J, Han A. Microfluidic compartmentalized co-culture platform for CNS axon myelination research. Biomed Microdevices. 2009;11(6):1145-1153.

[79]

Gur RE, Gur RC. Functional magnetic resonance imaging in schizophrenia. Dialogues Clin Neurosci. 2010;12(3):333-343.

[80]

Shi M, Majumdar D, Gao Y, et al. Glia co-culture with neurons in microfluidic platforms promotes the formation and stabilization of synaptic contacts. Lab Chip. 2013;13(15):3008-3021.

[81]

Choi SH, Kim YH, Hebisch M, et al. A three-dimensional human neural cell culture model of Alzheimer’s disease. Nature. 2014;515(7526):274-278.

[82]

Robertson G, Bushell TJ, Zagnoni M. Chemically induced synaptic activity between mixed primary hippocampal co-cultures in a microfluidic system. Integr Biol. 2014;6(6):636-644.

[83]

Di Ruscio A, Patti F, Welner RS, Tenen DG, Amabile G. Multiple sclerosis: getting personal with induced pluripotent stem cells. Cell Death Dis. 2015;6(7):e1806.

[84]

Smith I, Haag M, Ugbode C, et al. Neuronal-glial populations form functional networks in a biocompatible 3D scaffold. Neurosci Lett. 2015;609:198-202.

[85]

Jacquet L, Neueder A, Földes G, et al. Three Huntington’s disease specific mutation-carrying human embryonic stem cell lines have stable number of CAG repeats upon in vitro differentiation into cardiomyocytes. PLoS ONE. 2015;10(5):e0126860.

[86]

Rasmussen MA, Hjermind LE, Hasholt LF, et al. Induced pluripotent stem cells (iPSCs) derived from a patient with frontotemporal dementia caused by a P301L mutation in microtubule-associated protein tau (MAPT). Stem Cell Res. 2016a;16(1):70-74.

[87]

Rasmussen MA, Hjermind LE, Hasholt LF, et al. Induced pluripotent stem cells (iPSCs) derived from a patient with frontotemporal dementia caused by a R406W mutation in microtubule-associated protein tau (MAPT). Stem Cell Res. 2016b;16(1):75-78.

[88]

Geuna S, Raimondo S, Fregnan F, Haastert-Talini K, Grothe C. In vitro models for peripheral nerve regeneration. Eur J Neurosci. 2016;43(3):287-296.

[89]

Madill M, Fitzgerald D, O’Connell KE, Dev KK, Shen S, FitzGerald U. In vitro and ex vivo models of multiple sclerosis. Drug Discov Today. 2016;21(9):1504-1511.

[90]

Krencik R, Seo K, van Asperen JV, et al. Systematic three-dimensional coculture rapidly recapitulates interactions between human neurons and astrocytes. Stem Cell Rep. 2017;9(6):1745-1753.

[91]

Park J, Wetzel I, Marriott I, et al. A 3D human triculture system modeling neurodegeneration and neuroinflammation in Alzheimer’s disease. Nat Neurosci. 2018;21(7):941-951.

[92]

Pansarasa O, Bordoni M, Drufuca L, et al. Lymphoblastoid cell lines as a model to understand amyotrophic lateral sclerosis disease mechanisms. Dis Model Mech. 2018;11(3):dmm031625.

[93]

Lemos A, Melo R, Preto AJ, Almeida JG, Moreira IS, Dias Soeiro Cordeiro MN. In silico studies targeting G-protein coupled receptors for drug research against Parkinson’s disease. Curr Neuropharmacol. 2018;16(6):786-848.

[94]

Sung JH, Wang Y, Shuler ML. Strategies for using mathematical modeling approaches to design and interpret multi-organ microphysiological systems (MPS). APL Bioeng. 2019;3(2):021501.

[95]

Sellgren CM, Gracias J, Watmuff B, et al. Increased synapse elimination by microglia in schizophrenia patient-derived models of synaptic pruning. Nat Neurosci. 2019;22(3):374-385.

[96]

Harischandra DS, Rokad D, Ghaisas S, et al. Enhanced differentiation of human dopaminergic neuronal cell model for preclinical translational research in Parkinson’s disease. Biochim Biophys Acta Mol basis Dis. 2020;1866(4):165533.

[97]

Allegra Mascaro AL, Falotico E, Petkoski S, et al. Experimental and computational study on motor control and recovery after stroke: toward a constructive loop between experimental and virtual embodied neuroscience. Front Syst Neurosci. 2020;14:31.

[98]

Alrashidi H, Eaton S, Heales S. Biochemical characterization of proliferative and differentiated SH-SY5Y cell line as a model for Parkinson’s disease. Neurochem Int. 2021;145:105009.

[99]

Kohli H, Kumar P, Ambasta RK. In silico designing of putative peptides for targeting pathological protein Htt in Huntington’s disease. Heliyon. 2021;7(2):e06088.

[100]

Kim EA, Jung KC, Sohn UD, Im C. Quantitative structure activity relationship between diazabicyclo [4.2.0] octanes derivatives and nicotinic acetylcholine receptor agonists. Korean J Physiol Pharmacol. 2009;13(1):55-59.

[101]

Choquet D, Sainlos M, Sibarita JB. Advanced imaging and labelling methods to decipher brain cell organization and function. Nat Rev Neurosci. 2021;22(4):237-255.

[102]

Sánchez-Dengra B, Gonzalez-Alvarez I, Bermejo M, Gonzalez-Alvarez M. Physiologically based pharmacokinetic (PBPK) modeling for predicting brain levels of drug in rat. Pharmaceutics. 2021;13(9):1402.

[103]

Sunildutt N, Parihar P, Chethikkattuveli Salih AR, Lee SH, Choi KH. Revolutionizing drug development: harnessing the potential of organ-on-chip technology for disease modeling and drug discovery. Front Pharmacol. 2023;14:1139229.

[104]

Köseoğlu AE, Zerin A, Tunç İ, et al. Comparing the impact of wild type and derived DBP allelic variants detected in the Turkish population on serum vitamin D levels by bioinformatics analysis. Hum Nutr Metab. 2024;36:200263.

[105]

Kellogg EA, Shaffer HB. Model organisms in evolutionary studies. Syst Biol. 1993;42(4):409-414.

[106]

Zacchigna S, de Almodovar CR, Carmeliet P. Similarities between angiogenesis and neural development: what small animal models can tell us. Curr Top Dev Biol. 2007;80:1-55.

[107]

Hubel DH, Wiesel TN. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol. 1962;160(1):106-154.

[108]

Mitchell AS, Thiele A, Petkov CI, et al. Continued need for non-human primate neuroscience research. Curr Biol. 2018;28(20):R1186-R1187.

[109]

Morata Tarifa C, López Navas L, Azkona G, Sánchez Pernaute R. Chimeras for the twenty-first century. Crit Rev Biotechnol. 2020;40(3):283-291.

[110]

Meredith GE, Kang UJ. Behavioral models of Parkinson’s disease in rodents: a new look at an old problem. Mov Disord. 2006;21(10):1595-1606.

[111]

Medeiros DDC, Lopes Aguiar C, Moraes MFD, Fisone G. Sleep disorders in rodent models of Parkinson’s disease. Front Pharmacol. 2019;10:1414.

[112]

Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology. 2008;33(2):320-331.

[113]

Peng X, Knouse JA, Hernon KM. Rabbit models for studying human infectious diseases. Comp Med. 2015;65(6):499-507.

[114]

Peeters MCE, Hekking JWM, van Straaten HWM, Shum ASW, Copp AJ. Relationship between altered axial curvature and neural tube closure in normal and mutant (curly tail) mouse embryos. Anat Embryol. 1996;193(2):123-130.

[115]

Stewart AM, Braubach O, Spitsbergen J, Gerlai R, Kalueff AV. Zebrafish models for translational neuroscience research: from tank to bedside. Trends Neurosci. 2014;37(5):264-278.

[116]

Holland LZ. Chapter 4—Invertebrate origins of vertebrate nervous systems. In: Kaas JH, ed. Evolutionary Neuroscience. 2nd ed. Academic Press; 2020:51-73.

[117]

Lacalli T. An evolutionary perspective on chordate brain organization and function: insights from amphioxus, and the problem of sentience. Philos Trans R Soc Lond Ser B Biol Sci. 2021;377(1844):20200520.

[118]

Kleinenberg N. Hydra: Eine Anatomisch-entwicklungsgeschichtliche Untersuchung. W. Engelmann; 1872.

[119]

Hertwig O, Hertwig R. Das Nervensystem und die Sinnesorgane der medusen. Vogel; 1878.

[120]

Parker GH. The Elementary Nervous System; 1919. https://philpapers.org/rec/PARTEN-2

[121]

Moroz LL. On the independent origins of complex brains and neurons. Brain Behav Evol. 2009;74(3):177-190.

[122]

Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H. An urbilaterian origin of the tripartite brain: developmental genetic insights from drosophila. Development. 2003;130(11):2365-2373.

[123]

Rahmani A, Chew YL. Investigating the molecular mechanisms of learning and memory using Caenorhabditis elegans. J Neurochem. 2021;159(3):417-451.

[124]

Van Damme S, De Fruyt N, Watteyne J, et al. Neuromodulatory pathways in learning and memory: lessons from invertebrates. J Neuroendocrinol. 2021;33(1):e12911.

[125]

Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118(2):401-415.

[126]

White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond Ser B Biol Sci. 1986;314(1165):1-340.

[127]

Cook SJ, Jarrell TA, Brittin CA, et al. Whole-animal connectomes of both Caenorhabditis elegans sexes. Nature. 2019;571(7763):63-71.

[128]

Bailey CH, Castellucci VF, Koester J, Chen M. Behavioral changes in aging Aplysia: a model system for studying the cellular basis of age-impaired learning, memory, and arousal. Behav Neural Biol. 1983;38(1):70-81.

[129]

Baxter DA, Byrne JH. Feeding behavior of Aplysia: a model system for comparing cellular mechanisms of classical and operant conditioning. Learn Mem. 2006;13(6):669-680.

[130]

Moroz LL, Edwards JR, Puthanveettil SV, et al. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell. 2006;127(7):1453-1467.

[131]

Moroz LL, Kohn AB. Single-neuron transcriptome and methylome sequencing for epigenomic analysis of aging. In: Tollefsbol TO, ed. Biological Aging: Methods and Protocols. Humana Press; 2013:323-352.

[132]

Greer JB, Schmale MC, Fieber LA. Whole-transcriptome changes in gene expression accompany aging of sensory neurons in Aplysia californica. BMC Genomics. 2018;19(1):529.

[133]

Levy N. The use of animal as models: ethical considerations. Int J Stroke. 2012;7(5):440-442.

[134]

Gossel PP. William Henry Welch and the antivivisection legislation in the District of Columbia, 1896–1900. J Hist Med Allied Sci. 1985;40(4):397-419.

[135]

Lederer S, Davis AB. Subjected to science: human experimentation in America before the second world war. Hist Rev New Books. 1995;24(1):13.

[136]

Ferdowsian HR, Beck N. Ethical and scientific considerations regarding animal testing and research. PLoS ONE. 2011;6(9):e24059.

[137]

VandeWoude S, Rollin BE. Practical Considerations in Regenerative Medicine Research: IACUCs, Ethics, and the Use of Animals in Stem Cell Studies; 2010. https://www.wellbeingintlstudiesrepository.org/bioamres/4

[138]

National Research Council (US) Committee to Update Science, Medicine, and Animals. Regulation of Animal Research. National Academies Press (US); 2004. https://www.ncbi.nlm.nih.gov/books/NBK24650/

[139]

Singh J. The national centre for the replacement, refinement, and reduction of animals in research. J Pharmacol Pharmacother. 2012;3(1):87-89.

[140]

Marinou KA, Dontas IA. European Union legislation for the welfare of animals used for scientific purposes: areas identified for further discussion. Animals. 2023;13(14):2367.

[141]

Griffin G. Establishing a three Rs Programme at the Canadian Council on animal care. Altern Lab Anim. 2009;37(suppl. 2):63-67.

[142]

Hubrecht R. Revised Australian code for the care and use of animals for scientific purposes. Anim Welf. 2013;22(4):491.

[143]

MacArthur Clark JA, Sun D. Guidelines for the ethical review of laboratory animal welfare People’s Republic of China National Standard GB/T 35892-2018 [issued 6 February 2018 effective from 1 September 2018]. Anim Models Expe Med. 2020;3(1):103-113.

[144]

National Research Council; Division on Earth and Life Studies; Institute for Laboratory Animal Research; International Workshop on the Development of Science-Based Guidelines for Laboratory Animal Care Program Committee. The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop. National Academies Press; 2004.

[145]

Gregory NG. Physiology and Behaviour of Animal Suffering; n.d. Accessed April 9, 2023. https://books.google.com/books/about/Physiology_and_Behaviour_of_Animal_Suffe.html?id=0bOZocGJMaAC

[146]

Balcombe JP, Barnard ND, Sandusky C. Laboratory Routines Cause Animal Stress. American Association for Laboratory Animal Science; 2004. https://www.ingentaconnect.com/content/aalas/jaalas/2004/00000043/00000006/art00009

[147]

McMillan FD. Mental Health and Well-being in Animals, 2nd ed. n.d. Accessed April 9, 2023. https://books.google.com/books/about/Mental_Health_and_Well_being_in_Animals.html?id=Lge9DwAAQBAJ

[148]

Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. JAMA. 2006;296(14):1727-1732.

[149]

Perel P, Roberts I, Sena E, et al. Comparison of treatment effects between animal experiments and clinical trials: systematic review. Br Med J. 2007;334(7586):197.

[150]

Langley G, Evans T, Holgate ST, Jones A. Replacing animal experiments: choices, chances and challenges. BioEssays. 2007;29(9):918-926.

[151]

National Research Council, Division on Earth and Life Studies, Institute for Laboratory Animal Research, Board on Environmental Studies and Toxicology, Committee on Toxicity Testing and Assessment of Environmental Agents. Toxicity Testing in the 21st Century; n.d. Accessed April 18, 2023. https://books.google.com/books/about/Toxicity_Testing_in_the_21st_Century.html?id=3AWfAwAAQBAJ

[152]

Byers AM, Tapia TM, Sassano ER, Wittman V. In vitro antibody response to tetanus in the MIMIC system is a representative measure of vaccine immunogenicity. Biologicals. 2009;37(3):148-151.

[153]

Higbee RG, Byers AM, Dhir V, et al. An immunologic model for rapid vaccine assessment—a clinical trial in a test tube. Altern Lab Anim. 2009;37(suppl. 1):19-27.

[154]

Akhtar A. The flaws and human harms of animal experimentation. Camb Q Healthc Ethics. 2015;24(4):407-419.

[155]

Hoarau-Véchot J, Rafii A, Touboul C, Pasquier J. Halfway between 2D and animal models: are 3D cultures the ideal tool to study cancer-microenvironment interactions? Int J Mol Sci. 2018;19(1):181.

[156]

Jensen C, Teng Y. Is it time to start transitioning from 2D to 3D cell culture? Front Mol Biosci. 2020;7:33.

[157]

Chiaradia I, Lancaster MA. Brain organoids for the study of human neurobiology at the interface of in vitro and in vivo. Nat Neurosci. 2020;23(12):1496-1508.

[158]

Amirifar L, Shamloo A, Nasiri R, et al. Brain-on-a-chip: recent advances in design and techniques for microfluidic models of the brain in health and disease. Biomaterials. 2022;285:121531.

[159]

Li Z, Zhao Y, Lv X, Deng Y. Integrated brain on a chip and automated organ-on-chips systems. Interdiscip Med. 2023;1(1):e20220002.

[160]

Cekanova M, Rathore K. Animal models and therapeutic molecular targets of cancer: utility and limitations. Drug Des Devel Ther. 2014;8:1911-1922.

[161]

Voskoglou-Nomikos T, Pater JL, Seymour L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res. 2003;9(11):4227-4239.

[162]

Mak IW, Evaniew N, Ghert M. Lost in translation: animal models and clinical trials in cancer treatment. Am J Transl Res. 2014;6(2):114-118.

[163]

Schwartz MP, Hou Z, Propson NE, et al. Human pluripotent stem cell-derived neural constructs for predicting neural toxicity. Proc Natl Acad Sci USA. 2015;112:12516-12521.

[164]

Bershteyn M, Nowakowski TJ, Pollen AA, et al. Human iPSC-derived cerebral organoids model cellular features of lissencephaly and reveal prolonged mitosis of outer radial glia. Cell Stem Cell. 2017;20(4):435-449.e4.

[165]

Lancaster MA, Renner M, Martin C-A, et al. Cerebral organoids model human brain development and microcephaly. Nature. 2013;501(7467):373-379.

[166]

Lippmann ES, Al-Ahmad A, Palecek SP, Shusta EV. Modeling the blood–brain barrier using stem cell sources. Fluids Barriers CNS. 2013;10(1):2.

[167]

Israel MA, Yuan SH, Bardy C, et al. Probing sporadic and familial Alzheimer’s disease using induced pluripotent stem cells. Nature. 2012;482(7384):216-220.

[168]

Marchetto MCN, Carromeu C, Acab A, et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell. 2010;143(4):527-539.

[169]

El Aissouq A, Bouachrine M, Ouammou A, Khalil F. Homology modeling, virtual screening, molecular docking, molecular dynamic (MD) simulation, and ADMET approaches for identification of natural anti-Parkinson agents targeting MAO-B protein. Neurosci Lett. 2022;786:136803.

[170]

Patel HM, Noolvi MN, Sharma P, et al. Quantitative structure–activity relationship (QSAR) studies as strategic approach in drug discovery. Med Chem Res. 2014;23(12):4991-5007.

[171]

Cherry AL, Wheeler MJ, Mathisova K, Di Miceli M. In silico analyses of the involvement of GPR55, CB1R and TRPV1: response to THC, contribution to temporal lobe epilepsy, structural modeling and updated evolution. Front Neuroinform. 2024;18:1294939.

[172]

Köseoğlu AE, Paltacı S, Can H, et al. Applicability evaluation of mtDNA based molecular identification in mosquito species/subspecies/biotypes collected from Thessaloniki, Greece. Vet Parasitol Reg Stud Rep. 2023;41:100869.

[173]

Álvarez-Carretero S, Kapli P, Yang Z. Beginner’s guide on the use of PAML to detect positive selection. Mol Biol Evol. 2023;40(4):msad041.

[174]

Szathmáry E, Szathmáry Z, Ittzés P, et al. In silico evolutionary developmental neurobiology and the origin of natural language. In: Lyon C, Nehaniv CL, Cangelosi A, eds. Emergence of Communication and Language. Springer; 2007:151-187.

[175]

Husain A, Meenakshi DU, Ahmad A, Shrivastava N, Khan SA. A review on alternative methods to experimental animals in biological testing: recent advancement and current strategies. J Pharm Bioallied Sci. 2023;15(4):165-171.

[176]

Lou Y-R, Leung AW. Next generation organoids for biomedical research and applications. Biotechnol Adv. 2018;36(1):132-149.

[177]

Huang Y, Huang Z, Tang Z, et al. Research progress, challenges, and breakthroughs of organoids as disease models. Front Cell Dev Biol. 2021;9:740574.

[178]

Mollaki V. Ethical challenges in organoid use. Biotech. 2021;10(3):12.

[179]

Fisher J, Henzinger TA. Executable cell biology. Nat Biotechnol. 2007;25(11):1239-1249.

[180]

Jean-Quartier C, Jeanquartier F, Jurisica I, Holzinger A. In silico cancer research towards 3R. BMC Cancer. 2018;18(1):408.

[181]

Houssein EH, Hosney ME, Emam MM, Younis EMG, Ali AA, Mohamed WM. Soft computing techniques for biomedical data analysis: open issues and challenges. Artif Intell Rev. 2023;56(2):2599-2649.

[182]

Park G, Rim YA, Sohn Y, Nam Y, Ju JH. Replacing animal testing with stem cell-organoids: advantages and limitations. Stem Cell Rev Rep. 2024;20(6):1375-1386.

[183]

Mahalmani V, Prakash A, Medhi B. Do alternatives to animal experimentation replace preclinical research? Indian J Pharm. 2023;55(2):71-75.

RIGHTS & PERMISSIONS

2024 The Author(s). Animal Models and Experimental Medicine published by John Wiley & Sons Australia, Ltd on behalf of The Chinese Association for Laboratory Animal Sciences.

AI Summary AI Mindmap
PDF (1860KB)

200

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/