A Comprehensive Behavioral Test Battery to Assess Learning and Memory in 129S6/Tg2576 Mice

Wolf, Andrea; Bauer, Björn; Abner, Erin L.; Ashkenazy-Frolinger, Tal; Hartz, Anika M. S.

doi:10.1371/journal.pone.0147733

Cited by 282Alzheimer's disease research and treatmentsMemory and Neural MechanismsDementia and Cognitive Impairment Research

A Comprehensive Behavioral Test Battery to Assess Learning and Memory in 129S6/Tg2576 Mice

Open access

Wolf, Andrea, Bauer, Björn, Abner, Erin L., Ashkenazy-Frolinger, Tal, Hartz, Anika M. S.·2016·PLOS ONE

DOI 10.1371/journal.pone.0147733PMC PMC4726499

Open this paper in CoChat — free account Open PDF

Abstract

Transgenic Tg2576 mice overexpressing human amyloid precursor protein (hAPP) are a widely used Alzheimer's disease (AD) mouse model to evaluate treatment effects on amyloid beta (Aβ) pathology and cognition. Tg2576 mice on a B6;SJL background strain carry a recessive rd1 mutation that leads to early retinal degeneration and visual impairment in homozygous carriers. This can impair performance in behavioral tests that rely on visual cues, and thus, affect study results. Therefore, B6;SJL/Tg2576 mice were systematically backcrossed with 129S6/SvEvTac mice resulting in 129S6/Tg2576 mice that lack the rd1 mutation. 129S6/Tg2576 mice do not develop retinal degeneration but still show Aβ accumulation in the brain that is comparable to the original B6;SJL/Tg2576 mouse. However, comprehensive studies on cognitive decline in 129S6/Tg2576 mice are limited. In this study, we used two dementia mouse models on a 129S6 background--scopolamine-treated 129S6/SvEvTac mice (3-5 month-old) and transgenic 129S6/Tg2576 mice (11-13 month-old)-to establish a behavioral test battery for assessing learning and memory. The test battery consisted of five tests to evaluate different aspects of cognitive impairment: a Y-Maze forced alternation task, a novel object recognition test, the Morris water maze, the radial arm water maze, and a Y-maze spontaneous alternation task. We first established this behavioral test battery with the scopolamine-induced dementia model using 129S6/SvEvTac mice and then evaluated 129S6/Tg2576 mice using the same testing protocol. Both models showed distinctive patterns of cognitive impairment. Together, the non-invasive behavioral test battery presented here allows detecting cognitive impairment in scopolamine-treated 129S6/SvEvTac mice and in transgenic 129S6/Tg2576 mice. Due to the modular nature of this test battery, more behavioral tests, e.g. invasive assays to gain additional cognitive information, can easily be added.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0147733

Cites

89 of 89 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

For behavioral tests, exclusion criteria were pre-established following published guidance.
“For behavioral tests, exclusion criteria were pre-established following published guidance 71,79,80.”
From Exercise hormone irisin is a critical regulator of cognitive function (2021) · cites this paper as [71]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Clinical diagnosis of Alzheimer's disease: Report of the NINCDS‐ADRDA Work Group* under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984) · Neurology · doi:10.1212/wnl.34.7.939 · Cited by 27,915 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
The cholinergic hypothesis of geriatric memory dysfunction
Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982) · Science · doi:10.1126/science.7046051 · Cited by 5,545 · cited 1× · see citing works
“Scopolamine-induced dementia has been studied in rodents and humans, but no work has been published on scopolamine-induced dementia in 129S6 mice [42, 43].”
Background
2016 Alzheimer's disease facts and figures
Alzheimer's Association (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.03.001 · Cited by 5,069 · see citing works
Morris water maze: procedures for assessing spatial and related forms of learning and memory
Vorhees, C. V., & Williams, M. T. (2006) · Nature Protocols · doi:10.1038/nprot.2006.116 · Cited by 4,629 · see citing works
Correlative Memory Deficits, Aβ Elevation, and Amyloid Plaques in Transgenic Mice
Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., & Cole, G. (1996) · Science · doi:10.1126/science.274.5284.99 · Cited by 4,210 · cited 4× · see citing works
“B6;SJL/Tg2576 mice overexpress the human amyloid precursor protein (hAPP) 695 isoform that harbors the Swedish double mutation found in some cases of familial AD [5].”
BackgroundMethodInfluential
Hearing loss and cognitive decline in older adults
Lin, F. R., Yaffe, K., Xia, J., Xue, Q.-L., Harris, T. B., Purchase-Helzner, E., Satterfield, S., Ayonayon, H. N., Ferrucci, L., Simonsick, E. M., et al. (2013) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2013.1868 · Cited by 4,017 · see citing works
2013 Alzheimer's disease facts and figures
Thies, W. H., & Bleiler, L. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.02.003 · Cited by 3,331 · see citing works
A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data
Ennaceur, A., & Delacour, J. (1988) · Behavioural Brain Research · doi:10.1016/0166-4328(88)90157-x · Cited by 3,223 · cited 2× · see citing works
“Sitting or leaning on the object was not considered object exploration [23, 24].”
Background
The novel object recognition memory: neurobiology, test procedure, and its modifications
Antunes, M., & Biala, G. (2012) · Cognitive Processing · doi:10.1007/s10339-011-0430-z · Cited by 2,390 · cited 1× · see citing works
“The novel object recognition test is used to assess recognition memory in mice and is based on the inherent tendency of rodents to explore a novel object longer than a familiar one [38].”
Method
Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease
Morgan, D., Diamond, D. M., Gottschall, P. E., Ugen, K. E., Dickey, C. A., Hardy, J., Duff, K., Jantzen, P. T., DiCarlo, G., Wilcock, D. M., et al. (2000) · Nature · doi:10.1038/35050116 · Cited by 1,488 · see citing works
The Clinical Diagnosis of Alzheimer's Disease
Wade, J. P. H., Mirsen, T. R., Hachinski, V. C., Fisman, M., Lau, C. S., & Merskey, H. (1987) · Archives of Neurology · doi:10.1001/archneur.1987.00520130016010 · Cited by 1,416 · see citing works
Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes
Holcomb, L., Gordon, M. N., McGowan, E., Yu, X., Benkovic, S., Jantzen, P., Wright, K., Saad, I., Mueller, R., Morgan, D., et al. (1998) · Nature Medicine · doi:10.1038/nm0198-097 · Cited by 1,386 · cited 1× · see citing works
“Overall, the available data from Tg2576 mice on a B6;SJL or a mixed C57 background vary widely, with some studies showing memory deficits as early as 3 months of age [28, 83], while others detect no difference in mice at various ages [17, 28, 44–46].”
Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies
Crawley, J. N., Belknap, J. K., Collins, A. C., Crabbe, J. C., Frankel, W. N., Henderson, N. D., HITZEMANN, R. J., Maxson, S. C., Miner, L. L., Silva, A. J., et al. (1997) · Psychopharmacology · doi:10.1007/s002130050327 · Cited by 1,372 · cited 1× · see citing works
“Mice had in average less than 24 arm entries over the course of 5 minutes [33, 34, 63, 65].”
Background
Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'
Bevins, R. A., & Besheer, J. (2006) · Nature Protocols · doi:10.1038/nprot.2006.205 · Cited by 1,278 · cited 3× · see citing works
“Object interaction [%] for the novel object was calculated as (novel object interaction x 100) / (sample object interaction + novel object interaction) [25].”
Background
Age-Dependent Changes in Brain, CSF, and Plasma Amyloid β Protein in the Tg2576 Transgenic Mouse Model of Alzheimer's Disease
Kawarabayashi, T., Younkin, L. H., Saido, T. C., Shoji, M., Ashe, K. H., & Younkin, S. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00372.2001 · Cited by 1,053 · see citing works
2014 Alzheimer's disease facts and figures
Alzheimer's Association (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.02.001 · Cited by 1,032 · see citing works
T-maze alternation in the rodent
Deacon, R. M. J., & Rawlins, J. N. P. (2006) · Nature Protocols · doi:10.1038/nprot.2006.2 · Cited by 901 · cited 2× · see citing works
“Alternation tasks measure the disposition of rodents to explore new environments and are used to evaluate working memory and exploratory behavior [23, 37].”
BackgroundMethod
The neurobiological basis of spontaneous alternation
Lalonde, R. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00041-0 · Cited by 842 · cited 1× · see citing works
“Overall, mice in this study showed between 22 and 35 arm entries over the course of 5 min, which is low compared to literature values of other mouse strains, and might indicate anxiety [33, 34, 63, 64].”
Result
Retinal degeneration mutants in the mouse
Chang, B., Hawes, N. L., Hurd, R. E., Davisson, M. T., Nusinowitz, S., & Heckenlively, J. R. (2002) · Vision Research · doi:10.1016/s0042-6989(01)00146-8 · Cited by 840 · see citing works
Neurofibrillary tangles of Alzheimer disease share antigenic determinants with the axonal microtubule-associated protein tau (tau)
Wood, J. G., Mirra, S. S., Pollock, N. J., & Binder, L. I. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.11.4040 · Cited by 749 · cited 1× · see citing works
“AD is characterized by accumulation of amyloid beta (A β ) and tau protein in the brain, which results in neurodegeneration followed by progressive cognitive decline [2 – 4].”
Background
The validity of scopolamine as a pharmacological model for cognitive impairment: A review of animal behavioral studies
Klinkenberg, I., & Blokland, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.04.001 · Cited by 714 · cited 1× · see citing works
“Scopolamine-induced dementia has been studied in rodents and humans, but no work has been published on scopolamine-induced dementia in 129S6 mice [42, 43].”
Background
The Relationship between Aβ and Memory in the Tg2576 Mouse Model of Alzheimer's Disease
Westerman, M. A., Cooper-Blacketer, D., Mariash, A., Kotilinek, L., Kawarabayashi, T., Younkin, L. H., Carlson, G. A., Younkin, S. G., & Ashe, K. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01858.2002 · Cited by 714 · see citing works
Functional Alterations in Memory Networks in Early Alzheimer’s Disease
Sperling, R. A., Dickerson, B. C., Pihlajamaki, M. M., Vannini, P., LaViolette, P. S., Vitolo, O. V., Hedden, T., Becker, J. A., Rentz, D. M., Selkoe, D. J., et al. (2010) · NeuroMolecular Medicine · doi:10.1007/s12017-009-8109-7 · Cited by 587 · cited 1× · see citing works
“The radial arm water maze test is used to assess episodic-like memory in rodents, which is one of the earliest clinical symptoms of AD [29, 39, 73, 74].”
Method
Intermittent fasting and caloric restriction ameliorate age-related behavioral deficits in the triple-transgenic mouse model of Alzheimer's disease
Halagappa, V. K. M., Guo, Z., Pearson, M., Matsuoka, Y., Cutler, R. G., LaFerla, F. M., & Mattson, M. P. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.12.019 · Cited by 580 · cited 1× · see citing works
“Fourth, we omitted tests involving food restriction, since this can influence Aβ levels and cognitive performance in mouse AD models [61, 62].”
Method
The use of behavioral test batteries: Effects of training history
McIlwain, K. L., Merriweather, M. Y., Yuva-Paylor, L. A., & Paylor, R. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00528-5 · Cited by 579 · cited 2× · see citing works
“Therefore, the little object interaction could be in part due to the specific genetic background of the mice tested [33, 34, 57 – 59, Third, another potential reason why the trends were not statistically significant could be due to the similarity of the objects used in this test.”
Background
The Neuropsychological Profile of Alzheimer DiseasePreprint
Weıntraub, S., Wicklund, A. H., & Salmon, D. P. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006171 · Cited by 569 · see citing works
Attenuation of scopolamine-induced impairment of spontaneous alternation behaviour by antagonist but not inverse agonist and agonist ?-carbolines
Sarter, M. F., Bodewitz, G., & Stephens, D. (1988) · Psychopharmacology · doi:10.1007/bf00212843 · Cited by 533 · cited 1× · see citing works
“…in learning memory (Morris and radial arm water maze), working memory (alternation), object discrimination (novel object recognition), spatial memory (Morris and radial arm water maze), long-term memory (radial arm water maze), and episodic-like memory (radial arm water maze) [24, 29, 35, 51 – 53].”
Background
Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins
Hsiao, K., Borchelt, D., Olson, K., Johannsdottir, R., Kitt, C. A., Yunis, W. S., Xu, S., Eckman, C., Younkin, S. G., Price, D., et al. (1995) · Neuron · doi:10.1016/0896-6273(95)90107-8 · Cited by 519 · cited 1× · see citing works
“Spontaneous Alternation [%] was defined as consecutive entries in 3 different arms (ABC), divided by the number of possible alternations (total arm entries minus 2; [30]).”
Background
Differential effect of the rd mutation on rods and cones in the mouse retina.
Carter‐Dawson, L. D., LaVail, M. M., & Sidman, R. L. (1978) · PubMed · Cited by 495 · see citing works
Caffeine protects Alzheimer’s mice against cognitive impairment and reduces brain β-amyloid production
Arendash, G. W., Schleif, W. S., Rezai-Zadeh, K. P., Jackson, E. K., Zacharia, L. C., Cracchiolo, J. R., Shippy, D. C., & Tan, J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.07.021 · Cited by 459 · cited 1× · see citing works
“[81] showed impaired memory in Tg (APPsw) mice at 8–9 months of age.”
Background
Handbook Of Behavioral Neuroscience
(2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(08)00237-3 · Cited by 425 · see citing works
Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: Relationships to β-amyloid deposition and neurotransmitter abnormalities
Savonenko, A. V., Xu, G. M., Melnikova, T., Morton, J. L., Gonzales, V., Wong, M. P., Price, D. L., Tang, F., Markowska, A. L., & Borchelt, D. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.10.022 · Cited by 396 · cited 4× · see citing works
“To determine long-term memory, entries into the target arm of the previous day’s first trial were also analyzed for days 2–12 [29].”
BackgroundMethodInfluential
Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage.
Wilcock, D. M., Rojiani, A. M., Rosenthal, A., Subbarao, S., Freeman, M. J., Gordon, M. N., & Morgan, D. (2004) · Journal of Neuroinflammation · doi:10.1186/1742-2094-1-24 · Cited by 388 · see citing works
Behavioral changes in transgenic mice expressing both amyloid precursor protein and presenilin-1 mutations: lack of association with amyloid deposits
Holcomb, L. A., Gordon, M. N., Jantzen, P., Hsiao, K., Duff, K., & Morgan, D. (1999) · Behavior Genetics · doi:10.1023/a:1021691918517 · Cited by 353 · cited 3× · see citing works
“B6;SJL/Tg2576 mice have memory impairment starting at about 6 months of age [7], but in some studies memory impairment could not be reproduced [31, 44, 46].”
BackgroundResult
Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses
Owen, E. H., Logue, S. F., Rasmussen, D. L., & Wehner, J. M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00165-6 · Cited by 347 · see citing works
Caloric restriction attenuates β‐amyloid neuropathology in a mouse model of Alzheimer's disease
Wang, J., Ho, L., Qin, W., Rocher, A. B., Seror, I., Humala, N., Maniar, K. P., Dolios, G., Wang, R., Hof, P. R., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-3182fje · Cited by 317 · cited 1× · see citing works
“Fourth, we omitted tests involving food restriction, since this can influence Aβ levels and cognitive performance in mouse AD models [61, 62].”
Method
Abnormal anxiety‐related behavior in serotonin transporter null mutant mice: the influence of genetic background
Holmes, A., Li, Q., Murphy, D. L., Gold, E. N., & Crawley, J. N. (2003) · Genes Brain & Behavior · doi:10.1046/j.1601-1848.2003.00050.x · Cited by 312 · cited 2× · see citing works
“Mice had in average less than 24 arm entries over the course of 5 minutes [33, 34, 63, 65].”
BackgroundResult
Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study
Mandillo, S., Tucci, V., Hölter, S. M., Méziane, H., Banchaabouchi, M. A., Kallnik, M., Lad, H. V., Nolan, P. M., Ouagazzal, A., Coghill, E. L., et al. (2008) · Physiological Genomics · doi:10.1152/physiolgenomics.90207.2008 · Cited by 286 · cited 1× · see citing works
“…in learning memory (Morris and radial arm water maze), working memory (alternation), object discrimination (novel object recognition), spatial memory (Morris and radial arm water maze), long-term memory (radial arm water maze), and episodic-like memory (radial arm water maze) [24, 29, 35, 51 – 53].”
Background
Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice
Holmes, A., Wrenn, C. C., Harris, A. P., Thayer, K. E., & Crawley, J. N. (2002) · Genes Brain & Behavior · doi:10.1046/j.1601-1848.2001.00005.x · Cited by 275 · cited 3× · see citing works
“Mice had in average less than 24 arm entries over the course of 5 minutes [33, 34, 63, 65].”
BackgroundResult
Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice
Alamed, J., Wilcock, D. M., Diamond, D. M., Gordon, M. N., & Morgan, D. (2006) · Nature Protocols · doi:10.1038/nprot.2006.275 · Cited by 256 · cited 1× · see citing works
“…in learning memory (Morris and radial arm water maze), working memory (alternation), object discrimination (novel object recognition), spatial memory (Morris and radial arm water maze), long-term memory (radial arm water maze), and episodic-like memory (radial arm water maze) [24, 29, 35, 51 – 53].”
Background
Behavioral characterization of the Tg2576 transgenic model of Alzheimer's disease through 19 months
King, D. L., & Arendash, G. W. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00639-x · Cited by 240 · cited 3× · see citing works
“Since then, multiple studies have been conducted by this and other groups using B6;SJL/Tg2576 mice in the Morris water maze [7, 9, 28, 31].”
BackgroundResult
A Selective Allosteric Potentiator of the M 1 Muscarinic Acetylcholine Receptor Increases Activity of Medial Prefrontal Cortical Neurons and Restores Impairments in Reversal Learning
Shirey-Rice, J. K., Brady, A. E., Jones, P. J., Davis, A. A., Bridges, T. M., Kennedy, J. P., Jadhav, S. B., Menon, U. N., Xiang, Z., Watson, M. L., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3930-09.2009 · Cited by 237 · see citing works
PKC ε Activation Prevents Synaptic Loss, Aβ Elevation, and Cognitive Deficits in Alzheimer's Disease Transgenic Mice
Hongpaisan, J., Sun, M., & Alkon, D. L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5209-10.2011 · Cited by 231 · see citing works
Progressive and gender-dependent cognitive impairment in the APPSW transgenic mouse model for Alzheimer’s disease
King, D. L., Arendash, G. W., Crawford, F., Sterk, T., Menendez, J., & MULLAN, M. J. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00037-6 · Cited by 227 · see citing works
Intermediate- and Long-Term Recognition Memory Deficits in Tg2576 Mice Are Reversed with Acute Calcineurin Inhibition
Taglialatela, G., Hogan, D., Zhang, W.-R., & Dineley, K. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.034 · Cited by 217 · cited 3× · see citing works
“Mice with less than 7 s of total object interaction in either trial were excluded from the analysis [26].”
BackgroundMethod
Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains
Bouwknecht, J. A., & Paylor, R. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00200-0 · Cited by 209 · see citing works
The influence of visual ability on learning and memory performance in 13 strains of micePreprint
Brown, R. E., & Wong, A. A. (2007) · Learning & Memory · doi:10.1101/lm.473907 · Cited by 186 · see citing works
Behavioural profiles of inbred mouse strains used as transgenic backgrounds. II: cognitive tests
Brooks, S. P., Pask, T., Jones, L., & Dunnett, S. B. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00109.x · Cited by 177 · cited 2× · see citing works
“The behavior of mice can vary significantly by lineage, resulting in different cognitive outcomes for each strain [32 – 36].”
Background
A comparison of 129S2/SvHsd and C57BL/6JOlaHsd mice on a test battery assessing sensorimotor, affective and cognitive behaviours: implications for the study of genetically modified mice
Contet, C. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00231-5 · Cited by 176 · cited 3× · see citing works
“Mice had in average less than 24 arm entries over the course of 5 minutes [33, 34, 63, 65].”
BackgroundResult
The object recognition task in rats and mice: A simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity
Bertaina‐Anglade, V., Enjuanes, E., Morillon, D., & Rochelle, C. D. L. (2006) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2006.04.001 · Cited by 168 · cited 2× · see citing works
“Indeed, an extended intertrial interval can lead to low performance [25, 68].”
Background
Three weeks of running wheel exposure improves cognitive performance in the aged Tg2576 mouse
Nichol, K. E., Parachikova, A. I., & Cotman, C. W. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.06.027 · Cited by 160 · see citing works
Serotonergic and cholinergic involvement in habituation of activity and spontaneous alternation of rats in a maze.
Swonger, A. K., & Rech, R. H. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033690 · Cited by 159 · cited 1× · see citing works
“Spontaneous alternation using a Y-maze is a test for habituation and spatial working memory [37, 40].”
Method
Deglycosylated Anti-Amyloid-β Antibodies Eliminate Cognitive Deficits and Reduce Parenchymal Amyloid with Minimal Vascular Consequences in Aged Amyloid Precursor Protein Transgenic Mice
Wilcock, D. M., Alamed, J., Gottschall, P. E., Grimm, J., Rosenthal, A., Pons, J., Ronan, V., Symmonds, K., Gordon, M. N., & Morgan, D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0695-06.2006 · Cited by 154 · see citing works
Scopolamine-induced deficits in a two-trial object recognition task in mice
Dodart, J., Mathis, C., & Ungerer, A. (1997) · Neuroreport · doi:10.1097/00001756-199703240-00023 · Cited by 149 · cited 2× · see citing works
“First, the length of the intertrial interval determines the level of difficulty of this memory task, and thus, the performance in the object recognition test [26, 68, 69].”
BackgroundMethod
Cycloxygenase-2 activity promotes cognitive deficits but not increased amyloid burden in a model of Alzheimer’s disease in a sex-dimorphic pattern
Melnikova, T., Savonenko, A. V., Wang, Q., Liang, X., Hand, T. A., Wu, L., Kaufmann, W. E., Vehmas, A. K., & Andreasson, K. I. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.001 · Cited by 134 · cited 1× · see citing works
“The protocol for the forced alternation test was modified from Melnikova et al. [21].”
Method
A Noncompetitive BACE1 Inhibitor TAK-070 Ameliorates Aβ Pathology and Behavioral Deficits in a Mouse Model of Alzheimer's Disease
Fukumoto, H., Takahashi, H., Tarui, N., Matsui, J., Tomita, T., Hirode, M., Sagayama, M., Maeda, R., Kawamoto, M., Hirai, K., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2884-10.2010 · Cited by 132 · cited 1× · see citing works
“In the present novel object recognition test protocol, we incorporated a one-hour intertrial interval, which is a common intertrial interval in protocols of scopolamine-induced dementia and the Tg2576 model [20, 26, 66, 69, 70].”
Method
Age-dependent and -independent behavioral deficits in Tg2576 mice
Deacon, R. M. J., Cholerton, L. L., Talbot, K., Nair‐Roberts, R. G., Sanderson, D. J., Romberg, C., Koroś, E., Bornemann, K. D., & Rawlins, J. N. P. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.12.024 · Cited by 118 · cited 1× · see citing works
“B6;SJL/Tg2576 mice have memory impairment starting at about 6 months of age [7], but in some studies memory impairment could not be reproduced [31, 44, 46].”
Background
CCL2 Accelerates Microglia-Mediated Aβ Oligomer Formation and Progression of Neurocognitive Dysfunction
Kiyota, T., Yamamoto, M., Xiong, H., Lambert, M. P., Klein, W. L., Gendelman, H. E., Ransohoff, R. M., & Ikezu, T. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006197 · Cited by 114 · cited 1× · see citing works
“[76] showed cognitive deficits in 129-Sve/Tg2576 mice at 8–9 months of age using a 6-arm radial arm water maze, whereas mice at 2–3 months of age had no such deficits.”
Method
The aged mouse as a model of cognitive decline with special emphasis on studies in NMRI mice
Gower, A. J., & Lamberty, Y. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90132-a · Cited by 110 · see citing works
The spatio-temporal pattern of photoreceptor degeneration in the aged rd / rd mouse retina
Jimenez, A. J., García-Fernández, J. M., González, B., & Foster, R. G. (1996) · Cell and Tissue Research · doi:10.1007/s004410050579 · Cited by 100 · cited 1× · see citing works
“Since B6;SJL/Tg2576 mice carry the recessive Pde6brd1 (rd1) mutation, homozygous rd1 carriers have retinal degeneration and visual deficits at 7–9 weeks of age [12, 15, 47].”
Background
Behavioural differences between C57BL/6 and 129S6/SvEv strains are reinforced by environmental enrichment
Abramov, U., Puussaar, T., Raud, S., Kurrikoff, K., & Vasar, E. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.07.075 · Cited by 95 · cited 3× · see citing works
“Given that 129S6 mice naturally have high anxiety and low activity levels, which can lead to poor performance in behavioral tests such as passive avoidance or the Barnes maze, we selected tests that are minimally invasive and stressful [34, 57 – 60].”
Background
Which Memory Task for My Mouse? A Systematic Review of Spatial Memory Performance in the Tg2576 Alzheimer's Mouse Model
Stewart, S., Cacucci, F., & Lever, C. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-101827 · Cited by 94 · cited 1× · see citing works
“Although various tests have been used to characterize the behavioral/cognitive profile of B6;SJL/Tg2576 mice (reviewed in [11]), evaluating cognition in this AD model is challenging because one has to consider strain and model specific characteristics that can influence the results of cognitive testing.”
Method
Amelioration of early cognitive deficits by aged garlic extract in Alzheimer's transgenic mice
Chauhan, N. B., & Sandoval, J. (2007) · Phytotherapy Research · doi:10.1002/ptr.2122 · Cited by 84 · cited 1× · see citing works
“Since then, multiple studies have been conducted by this and other groups using B6;SJL/Tg2576 mice in the Morris water maze [7, 9, 28, 31].”
Result
Amyloid β inhibits retinoic acid synthesis exacerbating A lzheimer disease pathology which can be attenuated by an retinoic acid receptor α agonist
Goncalves, M. B. C. V., Clarke, E. E., Hobbs, C., Malmqvist, T., Deacon, R. M. J., Jack, J., & Corcoran, J. P. T. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12142 · Cited by 81 · see citing works
Interrogating rodents regarding their object and spatial memory
Clark, R. E., & Martin, S. J. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.08.014 · Cited by 81 · cited 2× · see citing works
“Alternation tasks measure the disposition of rodents to explore new environments and are used to evaluate working memory and exploratory behavior [23, 37].”
Background
Pharmacological Characterization of Memoquin, a Multi-Target Compound for the Treatment of Alzheimer's Disease
Capurro, V., Busquet, P., Lopes, J. P., Bertorelli, R., Tarozzo, G., Bolognesi, M. L., Piomelli, D., Reggiani, A. M., & Cavalli, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056870 · Cited by 81 · see citing works
Changes in behaviors of male C57BL/6J mice across adult life span and effects of dietary restriction
Fahlström, A., Zeberg, H., & Ulfhake, B. (2011) · AGE · doi:10.1007/s11357-011-9320-7 · Cited by 72 · see citing works
Ciproxifan, an H3 receptor antagonist, alleviates hyperactivity and cognitive deficits in the APPTg2576 mouse model of Alzheimer’s disease
Bardgett, M. E., Davis, N. N., Schultheis, P. J., & Griffith, M. S. (2010) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2010.10.008 · Cited by 67 · cited 4× · see citing works
“Second, we selected tests that have been established for the original B6;SJL/Tg2576 mouse model [5, 8 – 11, 31, 44, 45].”
BackgroundMethodInfluential
Dissociation of disinhibitory effects of scopolamine: Strain and task factors
Anisman, H. (1975) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(75)90182-3 · Cited by 64 · cited 3× · see citing works
“001) suggesting increased general activity produced by scopolamine as reported before (Fig 7B; [22, 41]).”
BackgroundMethod
Detecting spatial memory deficits beyond blindness in tg2576 Alzheimer mice
Yassine, N., Lazaris, A., Dorner‐Ciossek, C., Després, O., Meyer, L., Maître, M., Mensah‐Nyagan, A. G., Cassel, J., & Mathis, C. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.06.016 · Cited by 58 · cited 1× · see citing works
“However, retinal degeneration can confound experimental data in this test and introduce an impediment if outcomes are analyzed without considering the rd genotype [16, 17].”
Background
NIH Swiss and Black Swiss mice have retinal degeneration and performance deficits in cognitive tests.
Clapcote, S. J., Lazar, N. L., Bechard, A. R., Wood, G. A., & Roder, J. (2005) · PubMed · Cited by 51 · see citing works
Dissociation of the effects of scopolamine and d-amphetamine on a spontaneous alternation task
Kokkinidis, L., & Anisman, H. (1976) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(76)90081-2 · Cited by 50 · cited 1× · see citing works
“In contrast, decreased levels of spontaneous alternation were shown in Swiss-Webster mice dosed with 1 mg/kg scopolamine-HBr and in A/J, DBA/2J and C57BL/6J mice dosed with 10 mg/ kg scopolamine-HBr compared to saline-injected mice [22, 82].”
Method
Apparent Behavioral Benefits of Tau Overexpression in P301L Tau Transgenic Mice
Morgan, D., Munireddy, S., Alamed, J., DeLeon, J., Diamond, D. M., Bickford, P. C., Hutton, M. L., Lewis, J. M., McGowan, E. M., & Gordon, M. N. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-15407 · Cited by 46 · cited 1× · see citing works
“[45] utilized a novel 2-day protocol and showed that 8-month old C57/ Tg2576 mice had memory deficiencies.”
Method
The retinal degeneration (rd) gene seriously impairs spatial cognitive performance in normal and Alzheimer’s transgenic mice
Garcia, M. F., Gordon, M. N., Hutton, M. L., Lewis, J. M., McGowan, E. M., Dickey, C. A., Morgan, D., & Arendash, G. W. (2003) · Neuroreport · doi:10.1097/00001756-200401190-00015 · Cited by 45 · cited 1× · see citing works
“However, retinal degeneration can confound experimental data in this test and introduce an impediment if outcomes are analyzed without considering the rd genotype [16, 17].”
Background
Mice expressing the Swedish APP mutation on a 129 genetic background demonstrate consistent behavioral deficits and pathological markers of Alzheimer's disease
Rustay, N. R., Cronin, E. A., Curzon, P., Markosyan, S., Bitner, R. S., Ellis, T. A., Waring, J. F., Decker, M. W., Rueter, L. E., & Browman, K. E. (2009) · Brain Research · doi:10.1016/j.brainres.2009.11.040 · Cited by 38 · cited 7× · see citing works
“[18] showed that 7-month old 129S6/Tg2576 and B6;SJL/Tg2576 mice have comparable Aβ plasma concentrations and plaque loads in the brain.”
BackgroundMethodResultInfluential
Differential learning strategies in spatial and nonspatial versions of the Morris water maze in the C57BL/6J inbred mouse strain
Stavnezer, A. J., Hyde, L. A., Bimonte, H. A., Armstrong, C. M., & Denenberg, V. H. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00021-9 · Cited by 37 · see citing works
Behavioral consequences of ovarian atrophy and estrogen replacement in the APPswe mouse
Golub, M. S., Germann, S. L., Mercer, M., Gordon, M. N., Morgan, D., Mayer, L. P., & Hoyer, P. B. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.03.015 · Cited by 36 · cited 2× · see citing works
“At 6 – 12 months of age, B6;SJL/Tg2576 mice develop cognitive impairment [7], which has been the focus of numerous studies [5, 8 – 10].”
Background
Impaired hippocampal acetylcholine release parallels spatial memory deficits in Tg2576 mice subjected to basal forebrain cholinergic degeneration
Laursen, B., Mørk, A., Plath, N., Kristiansen, U., & Bastlund, J. F. (2013) · Brain Research · doi:10.1016/j.brainres.2013.10.055 · Cited by 33 · see citing works
Role of Cholinergic Neurotransmission in the Amygdala on Performances of Passive Avoidance Learning in Mice.
NOMURA, Y., Nishiyama, N., Saito, H., & Matsuki, N. (1994) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.17.490 · Cited by 33 · cited 1× · see citing works
“001) suggesting increased general activity produced by scopolamine as reported before (Fig 7B; [22, 41]).”
Background
Profiling psychomotor and cognitive aging in four-way cross mice
Sumien, N., Sims, M. N., Taylor, H., & Forster, M. J. (2006) · AGE · doi:10.1007/s11357-006-9015-7 · Cited by 32 · see citing works
Differential neuropsychopharmacological influences of naturally occurring tropane alkaloids anisodamine versus scopolamine
Zhang, W., Song, M., Cui, Y., Wang, H., Zhu, L., Niu, Y.-Y., Yang, L., Lu, Y., & Chen, H. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.07.048 · Cited by 29 · cited 2× · see citing works
“[71] showed that Kunming mice dosed with 0.”
Background
Reversal of scopolamine-induced spatial and recognition memory deficits in mice by novel multifunctional dimers bis-cognitins
Han, R.-W., Zhang, R.-S., Chang, M., Peng, Y.-L., Wang, P., Hu, S.-Q., Choi, C., Yin, M., Wang, R., & Han, Y. (2012) · Brain Research · doi:10.1016/j.brainres.2012.06.015 · Cited by 27 · cited 3× · see citing works
“[66] showed similar learning and memory deficits after treatment with 0.”
BackgroundMethod
Delay-Dependent Working Memory Impairment in Young-Adult and Aged 5-HT1BKO Mice as Assessed in a Radial-Arm Water MazePreprint
Wolff, M., Benhassine, N., Costet, P., Hen, R., Ségu, L., & Buhot, M.-C. (2003) · Learning & Memory · doi:10.1101/lm.60103 · Cited by 23 · cited 2× · see citing works
“) did not influence performance at a 5 min inter-trial interval, but impaired performance at a 60 min inter-trial interval [75].”
BackgroundMethod
Influence of trait anxiety on the effects of acute stress on learning and retention of the passive avoidance task in male and female mice
Navarro-Francés, C. I., & Arenas, M. C. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.02.009 · Cited by 23 · cited 1× · see citing works
“Given that 129S6 mice naturally have high anxiety and low activity levels, which can lead to poor performance in behavioral tests such as passive avoidance or the Barnes maze, we selected tests that are minimally invasive and stressful [34, 57 – 60].”
Effects of NK-4 in a Transgenic Mouse Model of Alzheimer's Disease
Ohta, H., Arai, S., Akita, K., Ohta, T., & Fukuda, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030007 · Cited by 16 · cited 5× · see citing works
“[20], who assessed behavior and cognition of 129S6/Tg2576 mice at 3, 6 and 12 months of age using various tests.”
BackgroundMethodInfluential
Chapter 5.5 Transgenic mouse models of Alzheimer's disease and episodic-like memory
Borchelt, D., & Savonenko, A. V. (2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(08)00230-0 · Cited by 4 · see citing works

Flagged first, then by citations

Sorted by citations

Inflammation and aging: signaling pathways and intervention therapies
Li, X., Li, C., Zhang, W., Wang, Y., Qian, P., & Huang, H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01502-8 · Cited by 1,443 · see citing works
Aged blood impairs hippocampal neural precursor activity and activates microglia via brain endothelial cell VCAM1
Yousef, H., Czupalla, C. J., Lee, D., Chen, M. B., Burke, A. N., Zera, K. A., Zandstra, J., Berber, E., Lehallier, B., Mathur, V., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0440-4 · Cited by 442 · see citing works
CD22 blockade restores homeostatic microglial phagocytosis in ageing brains
Pluvinage, J. V., Haney, M. S., Smith, B. A. H., Sun, J., Iram, T., Bonanno, L., Li, L., Lee, D. P., Morgens, D. W., Yang, A. C., et al. (2019) · Nature · doi:10.1038/s41586-019-1088-4 · Cited by 459 · see citing works
Exercise hormone irisin is a critical regulator of cognitive function
Islam, M. R., Valaris, S., Young, M. F., Haley, E. B., Luo, R., Bond, S. F., Mazuera, S., Kitchen, R. R., Caldarone, B. J., Bettio, L. E. B., et al. (2021) · Nature Metabolism · doi:10.1038/s42255-021-00438-z · Cited by 403 · see citing works
Novel Object Recognition and Object Location Behavioral Testing in Mice on a Budget
Denninger, J. K., Smith, B. M., & Kirby, E. D. (2018) · Journal of Visualized Experiments · doi:10.3791/58593 · Cited by 273 · see citing works
Biphenyl-3-oxo-1,2,4-triazine linked piperazine derivatives as potential cholinesterase inhibitors with anti-oxidant property to improve the learning and memory
Tripathi, P. N., Srivastava, P., Sharma, P. A., Tripathi, M. K., Seth, A., Tripathi, A., Nand, S., Singh, S. P., & Shrivastava, S. K. (2018) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2018.12.017 · Cited by 210 · see citing works
“The “memory improvement score” can be calculated as % alternations = (Number of alternations/(total arm entries – 2))× 100 [52].”
Salidroside alleviates cognitive impairment by inhibiting ferroptosis via activation of the Nrf2/GPX4 axis in SAMP8 mice
Yang, S., Wang, L., Zeng, Y., Wang, Y., Pei, T., Xie, Z., Xiong, Q., Wei, H., Li, W., Li, J., et al. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154762 · Cited by 153 · see citing works
Sialic Acid and Sialylated Oligosaccharide Supplementation during Lactation Improves Learning and Memory in Rats
Oliveros, E., Vázquez, E., Barranco, A., Ramírez, M., Gruart, A., Delgado-Garcia, J. M., Buck, R. H., Rueda, R., & Martín, M. J. (2018) · Nutrients · doi:10.3390/nu10101519 · Cited by 134 · see citing works
“The Y maze with blocked arm test measures the ability of rodents to explore new environments and assesses exploratory behavior and memory [45].”
Background
Critical windows of early-life microbiota disruption on behaviour, neuroimmune function, and neurodevelopment
Lynch, C. M. K., Cowan, C. S. M., Bastiaanssen, T. F. S., Moloney, G. M., Theune, N., van de Wouw, M., Florensa-Zanuy, E., Ventura‐Silva, A. P., Codagnone, M. G., Villalobos-Manríquez, F., et al. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.12.008 · Cited by 133 · see citing works
“Alternations as a percentage of total possible alternations (number of arm entries minus 2) were used to index spatial working memory (Wolf et al., 2016).”
Bacteriophage-mediated manipulation of the gut microbiome – promises and presents limitations
Rasmussen, T. S., Koefoed, A. K., Jakobsen, R. R., Deng, L., Castro-Mejía, J. L., Brunse, A., Neve, H., Vogensen, F. K., & Nielsen, D. S. (2020) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaa020 · Cited by 122 · see citing works
Preclinical Models of Alzheimer's Disease: Relevance and Translational Validity
Mullane, K., & Williams, M. J. (2019) · Current Protocols in Pharmacology · doi:10.1002/cpph.57 · Cited by 126 · see citing works
“In a behavioral assessment of the 129S6/Tg2546 transgenic mouse, Wolf et al. (2016) used a battery of tests (Fig.”
MethodInfluential
Dysregulated Gut Homeostasis Observed Prior to the Accumulation of the Brain Amyloid-β in Tg2576 Mice
Honarpisheh, P., Reynolds, C. R., Conesa, M. P. B., Moruno-Manchon, J. F., Putluri, N., Bhattacharjee, M. B., Urayama, A., McCullough, L. D., & Ganesh, B. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051711 · Cited by 127 · see citing works
“Tg2576 mice develop cerebral Aβ aggregates, white matter injury, and cognitive impairment beginning around 9 months of age [32].”
Background
From Synapses to Circuits, Astrocytes Regulate Behavior
Lyon, K. A., & Allen, N. J. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.786293 · Cited by 117 · see citing works
Identification of a protective microglial state mediated by miR-155 and interferon-γ signaling in a mouse model of Alzheimer’s disease
Yin, Z., Herron, S., Silveira, S., Kleemann, K., Gauthier, C., Mallah, D., Cheng, Y., Margeta, M. A., Pitts, K. M., Barry, J.-L., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01355-y · Cited by 120 · see citing works
Intra‐gastrointestinal amyloid‐β1–42 oligomers perturb enteric function and induce Alzheimer's disease pathology
Sun, Y., Sommerville, N. R., Liu, J. Y. H., Ngan, M. P., Poon, D., Ponomarev, E. D., Lu, Z., Kung, J. S. C., & Rudd, J. A. (2020) · The Journal of Physiology · doi:10.1113/jp279919 · Cited by 116 · see citing works
“Other murine dementia models reported insignificant differences (Faucher et al. 2016; Wolf et al. 2016).”
Background
Cognitive and behavioral evaluation of nutritional interventions in rodent models of brain aging and dementia
Wahl, D., Coogan, S. C. P., Solon‐Biet, S. M., de Cabo, R., Haran, J. B., Raubenheimer, D., Cogger, V. C., Mattson, M. P., Simpson, S. J., & Couteur, D. G. L. (2017) · Clinical Interventions in Aging · doi:10.2147/cia.s145247 · Cited by 111 · see citing works
“After a brief training period, results are quantified by the number of errors (ie, incorrect arm entries) and the number of seconds the mouse takes to reach the escape platform.(49)”
Design and development of multitarget-directed N-Benzylpiperidine analogs as potential candidates for the treatment of Alzheimer's disease
Sharma, P. A., Tripathi, A., Tripathi, P. N., Prajapati, S. K., Seth, A., Tripathi, M. K., Srivastava, P., Tiwari, V., Krishnamurthy, S., & Shrivastava, S. K. (2019) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2019.02.030 · Cited by 102 · see citing works
Behavioural phenotypes in the cuprizone model of central nervous system demyelination.
Sen, M. K., Mahns, D., Coorssen, J., & Shortland, P. (2019) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.08.008 · Cited by 84 · see citing works
Ten Years of Tau-Targeted Immunotherapy: The Path Walked and the Roads Ahead
Novak, P., Kontsekova, E., Zilka, N., & Novak, M. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00798 · Cited by 87 · see citing works
Natural hypothalamic circuit dynamics underlying object memorization
Kosse, C., & Burdakov, D. (2019) · Nature Communications · doi:10.1038/s41467-019-10484-7 · Cited by 84 · see citing works
Adar3 Is Involved in Learning and Memory in Mice
Mladenova, D. N., Barry, G., Konen, L. M., Pineda, S. S., Guennewig, B., Avesson, L., Zinn, R., Schönrock, N., Bitar, M., Jonkhout, N., et al. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00243 · Cited by 82 · see citing works
Distinguishing normal brain aging from the development of Alzheimer's disease: inflammation, insulin signaling and cognition
Denver, P., & McClean, P. L. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.238608 · Cited by 85 · see citing works
“Some (Wolf et al., 2016; Portbury et al., 2017), but not all (Bizon et al., 2007) have observed learning and memory impairments in aged adult Tg2576 mice, while early cognitive deficits have been detected in the 3xTg AD model (Stover et al., 2015).”
Background
Design and development of molecular hybrids of 2-pyridylpiperazine and 5-phenyl-1,3,4-oxadiazoles as potential multifunctional agents to treat Alzheimer's disease
Tripathi, A., Choubey, P. K., Sharma, P. A., Seth, A., Tripathi, P. N., Tripathi, M. K., Prajapati, S. K., Krishnamurthy, S., & Shrivastava, S. K. (2019) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2019.111707 · Cited by 81 · see citing works
Effects of repetitive gentle handling of male C57BL/6NCrl mice on comparative behavioural test results
Ueno, H., Takahashi, Y., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2020) · Scientific Reports · doi:10.1038/s41598-020-60530-4 · Cited by 81 · see citing works
Effect of simultaneous testing of two mice in the tail suspension test and forced swim test
Ueno, H., Takahashi, Y., Murakami, S., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2022) · Scientific Reports · doi:10.1038/s41598-022-12986-9 · Cited by 81 · see citing works
Oral Administration of Alpha Linoleic Acid Rescues Aβ-Induced Glia-Mediated Neuroinflammation and Cognitive Dysfunction in C57BL/6N Mice
Ali, W., Ikram, M. A., Park, H. Y., Jo, M. G., Ullah, R., Ahmad, S., Abid, N. B., & Kim, M. O. (2020) · Cells · doi:10.3390/cells9030667 · Cited by 78 · see citing works
“For the evaluation of spatial working memory, the Y-Maze assembly was used, which was made of three arms and arranged in a Y-shaped manner with dimensions of 30 × 15 × 15 cm, with an indicator at the top [36].”
Method
Memory enhancing effects of BPN14770, an allosteric inhibitor of phosphodiesterase-4D, in wild-type and humanized mice
Zhang, C., Xu, Y., Chowdhary, A., Fox, D. N. A., Gurney, M. E., Zhang, H., Auerbach, B. D., Salvi, R., Yang, M., Li, G., et al. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0178-6 · Cited by 77 · see citing works
Novel Molecular Hybrids of N-Benzylpiperidine and 1,3,4-Oxadiazole as Multitargeted Therapeutics to Treat Alzheimer’s Disease
Sharma, P. A., Tripathi, A., Tripathi, P. N., Singh, S. S., Singh, S. P., & Shrivastava, S. K. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.9b00430 · Cited by 72 · see citing works
Lipocalin 2 contributes to brain iron dysregulation but does not affect cognition, plaque load, and glial activation in the J20 Alzheimer mouse model
Dekens, D. W., Naudé, P. J. W., Keijser, J. N., Boerema, A. S., Deyn, P. P. D., & Eisel, U. L. M. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1372-5 · Cited by 69 · see citing works
The role of perceived dignity and control in the wish to hasten death among advanced cancer patients: A mediation model
Monforte‐Royo, C., Crespo, I., Rodríguez‐Prat, A., Marimón, F., Porta-Sales, J., & Balaguer, A. (2018) · Psycho-Oncology · doi:10.1002/pon.4900 · Cited by 62 · see citing works
Neuroprotective effect of menaquinone-4 (MK-4) on transient global cerebral ischemia/reperfusion injury in rat
Moghaddam, B. F., & Fereidoni, M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0229769 · Cited by 61 · see citing works
“Based on the previous study, spontaneous alternation (%) as an index for short-term memory, was calculated by the ratio of actual alternations to possible alternations, multiplied by 100 [39].”
Method
A TNF receptor 2 agonist ameliorates neuropathology and improves cognition in an Alzheimer’s disease mouse model
Ortí-Casañ, N., Zuhorn, I. S., Naudé, P. J. W., Deyn, P. P. D., van Schaik, P. E. M., Wajant, H., & Eisel, U. L. M. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201137119 · Cited by 60 · see citing works
Surgery/Anesthesia disturbs mitochondrial fission/fusion dynamics in the brain of aged mice with postoperative delirium
Lu, Y., Chen, L., Ye, J., Chen, C., Zhou, Y., Li, K., Zhang, Z., & Peng, M. (2020) · Aging · doi:10.18632/aging.102659 · Cited by 60 · see citing works
“The Y maze test was performed as described in the previous studies with modifications [75, 76].”
Method
Design and development of 1,3,4-oxadiazole derivatives as potential inhibitors of acetylcholinesterase to ameliorate scopolamine-induced cognitive dysfunctions
Mishra, P., Sharma, P. A., Tripathi, P. N., Gupta, S. K., Srivastava, P., Seth, A., Tripathi, A., Krishnamurthy, S., & Shrivastava, S. K. (2019) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2019.103025 · Cited by 58 · see citing works
“The Y-maze test is the standard animal model used for evaluation of hippocampal-dependent short-term working memory in the rodents [47].”
Method
Inflammation promotes synucleinopathy propagation
Kim, T.-K., Bae, E.-J., Jung, B. C., Choi, M.-S., Shin, S. J., Park, S. J., Kim, J. T., Jung, M. K., Ulusoy, A., Song, M., et al. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00895-w · Cited by 58 · see citing works
“To measure the prefrontal cortex-and hippocampus-dependent spatial memory de ﬁ cits 16 , we tested the spontaneous alternation behavior (SAB) and continuous alternation (CA) of mice using a standard protocol 17 .”
Method
Trx-1 ameliorates learning and memory deficits in MPTP-induced Parkinson's disease model in mice
Zhang, X., Bai, L., Zhang, S., Zhou, X., Li, Y., & Bai, J. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.06.029 · Cited by 56 · see citing works
MouBeAT: A New and Open Toolbox for Guided Analysis of Behavioral Tests in Mice
Bello-Arroyo, E., Roque, H., Marcos, A., Orihuel, J., Higuera‐Matas, A., Desco, M., Caiolfa, V. R., Ambrosio, E., Lara‐Pezzi, E., & Gómez‐Gaviro, M. V. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00201 · Cited by 56 · see citing works
“In order to calculate the percentage of alternation between maze arms, we measured three consecutive entries in different arms divided by the total of entries minus 2 (Wolf et al., 2016).”
Method
Are some animal models more equal than others? A case study on the translational value of animal models of efficacy for Alzheimer's disease
Veening-Griffioen, D. H., Ferreira, G. S., van Meer, P. J. K., Boon, W., Wied, C. C. G., Moors, E. H. M., & Schellekens, H. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172524 · Cited by 57 · see citing works
“For complex diseases such as Alzheimer's disease one could consider a (properly designed) test battery of different (animal) models simulating different aspects of the disease (Stukalin and Einat, 2019; Webster et al., 2014; Wolf et al., 2016).”
Background
Sex Differences between Neuronal Loss and the Early Onset of Amyloid Deposits and Behavioral Consequences in 5xFAD Transgenic Mouse as a Model for Alzheimer’s Disease
Poon, C. H., Wong, S. T. N., Roy, J., Wang, Y., Chan, H. W. H., Steinbusch, H. W. M., Blokland, A., Temel, Y., Aquili, L., & Lim, L. W. (2023) · Cells · doi:10.3390/cells12050780 · Cited by 54 · see citing works
“The percentage of spontaneous alternation, which indicates the animal’s spatial working memory, was defined as the consecutive entries into the three arms divided by the number of possible alternations (total arm entry minus 2) [18].”
Background
5-Caffeoylquinic Acid Ameliorates Cognitive Decline and Reduces Aβ Deposition by Modulating Aβ Clearance Pathways in APP/PS2 Transgenic Mice
Ishida, K., Misawa, K., Nishimura, H., Hirata, T., Yamamoto, M., & Ota, N. (2020) · Nutrients · doi:10.3390/nu12020494 · Cited by 53 · see citing works
“The Y-maze test is a spatial learning task based on working memory [34], whereas the novel object recognition test evaluates the spatial and temporal context of object recognition and visual recognition memory [34,35].”
Method
Design, synthesis, and evaluation of N-benzylpyrrolidine and 1,3,4-oxadiazole as multitargeted hybrids for the treatment of Alzheimer's disease.
Choubey, P. K., Tripathi, A., Tripathi, M., Seth, A., & Shrivastava, S. (2021) · Bioorganic chemistry (Print) · doi:10.1016/j.bioorg.2021.104922 · Cited by 42 · see citing works
Neuroprotective effect of hesperidin against emamectin benzoate-induced neurobehavioral toxicity in rats
Noshy, P. A., & Azouz, R. A. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.106981 · Cited by 51 · see citing works
Therapeutic targeting of immunometabolism reveals a critical reliance on hexokinase 2 dosage for microglial activation and Alzheimer’s progression
Codocedo, J. F., Mera-Reina, C., Bor-Chian Lin, P., Fallen, P. B., Puntambekar, S. S., Casali, B. T., Jury-Garfe, N., Martinez, P., Lasagna-Reeves, C. A., & Landreth, G. E. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114488 · Cited by 52 · see citing works
“36 The partial loss of HK2 significantly improved the cognitive performance of the mice (Figure 2P).”
Microglia knockdown reduces inflammation and preserves cognition in diabetic animals after experimental stroke
Jackson, L., Dumanli, S., Johnson, M. H., Fagan, S. C., & Ergul, A. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01815-3 · Cited by 50 · see citing works
Effects of Long‐Term Treatment with a Blend of Highly Purified Olive Secoiridoids on Cognition and Brain ATP Levels in Aged NMRI Mice
Reutzel, M., Grewal, R., Silaidos, C. V., Zotzel, J., Marx, S. P., Tretzel, J., & Eckert, G. P. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/4070935 · Cited by 48 · see citing works
“Spontaneous alternation was determined using the formula (number of alternations/number of entries)/2 [36].”
Method
Phosphatidylserine-microbubble targeting-activated microglia/macrophage in inflammation combined with ultrasound for breaking through the blood–brain barrier
Zhao, R., Jiang, J., Li, H., Chen, M., Liu, R., Sun, S., Ma, D., Liang, X., & Wang, S. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1368-1 · Cited by 48 · see citing works
Curcumin-loaded self-nanomicellizing solid dispersion system: part II: in vivo safety and efficacy assessment against behavior deficit in Alzheimer disease
Parikh, A. R., Kathawala, K., Li, J.-T., Chen, C., Shan, Z., Cao, X., Zhou, X., & Garg, S. (2018) · Drug Delivery and Translational Research · doi:10.1007/s13346-018-0570-0 · Cited by 46 · see citing works
Formulation and Development of Curcumin–Piperine-Loaded S-SNEDDS for the Treatment of Alzheimer’s Disease
Ahmad, S., & Hafeez, A. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03089-7 · Cited by 45 · see citing works
Ameliorative effect of carvacrol against propiconazole-induced neurobehavioral toxicity in rats
Noshy, P. A., Elhady, M. A., Khalaf, A. A. A., Kamel, M. M., & Hassanen, E. I. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.05.005 · Cited by 45 · see citing works
Combining P301L and S320F tau variants produces a novel accelerated model of tauopathy
Koller, E. J., Gonzalez De La Cruz, E., Machula, T., Ibanez, K. R., Lin, W.-L., Williams, T., Riffe, C. J., Ryu, D., Strang, K. H., Liu, X., et al. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddz151 · Cited by 63 · see citing works
“Y maze testing was conducted as described previously (43).”
Method
Comparison of the Response of Male BALB/c and C57BL/6 Mice in Behavioral Tasks to Evaluate Cognitive Function
García, Y., & Esquivel, N. (2018) · Behavioral Sciences · doi:10.3390/bs8010014 · Cited by 43 · see citing works
Translational Assays for Assessment of Cognition in Rodent Models of Alzheimer’s Disease and Dementia
Shepherd, A. L., Tyebji, S., Hannan, A. J., & Burrows, E. L. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0837-1 · Cited by 42 · see citing works
“Finally, impaired vision has been reported in a number of mouse models due to A-induced retinal deterioration and mutation-background strain interactions (Wolf et al. 2016).”
Background
Kolaviron protects the brain in cuprizone-induced model of experimental multiple sclerosis via enhancement of intrinsic antioxidant mechanisms: Possible therapeutic applications?
Omotoso, G. O., Inelo, U. I., Arietarhire, L. O., Sulaimon, F. A., & Gbadamosi, I. (2018) · Pathophysiology · doi:10.1016/j.pathophys.2018.04.004 · Cited by 42 · see citing works
Cerebral Mitochondrial Function and Cognitive Performance during Aging: A Longitudinal Study in NMRI Mice
Reutzel, M., Grewal, R., Dilberger, B., Silaidos, C. V., Joppe, A., & Eckert, G. P. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/4060769 · Cited by 41 · see citing works
Neuropathological and Cognitive Effects Induced by CuO-NPs in Rats and Trials for Prevention Using Pomegranate Juice
Hassanen, E. I., Ibrahim, M. A., Hassan, A. M., Mehanna, S., Aljuaydi, S. H., & Issa, M. Y. (2021) · Neurochemical Research · doi:10.1007/s11064-021-03264-7 · Cited by 42 · see citing works
A small molecule ApoE4-targeted therapeutic candidate that normalizes sirtuin 1 levels and improves cognition in an Alzheimer’s disease mouse model
Campagna, J. J., Spilman, P. R., Jagodzinska, B. M., Bai, D., Hatami, A., Zhu, C., Bilousova, T. V., Jun, M., Elias, C. J., Pham, J. D., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-35687-8 · Cited by 39 · see citing works
Pseudomonas chlororaphis as a multiproduct platform: Conversion of glycerol into high-value biopolymers and phenazines
Meneses, L., Pereira, J. R., Sevrin, C., Grandfils, C., Paiva, A., Reis, M. A. M., & Freitas, F. (2019) · New Biotechnology · doi:10.1016/j.nbt.2019.10.002 · Cited by 39 · see citing works
Hepatitis B core VLP-based mis-disordered tau vaccine elicits strong immune response and alleviates cognitive deficits and neuropathology progression in Tau.P301S mouse model of Alzheimer’s disease and frontotemporal dementia
Ji, M., Xie, X.-X., Liu, D., Yu, X., Zhang, Y., Zhang, L. L., Wang, S., Huang, Y., & Liu, R. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0378-7 · Cited by 38 · see citing works
“culated as (actual alternations/maximum alternations) × 100% as described previously [28].”
Combined effects of aquaporin-4 and hypoxia produce age-related hydrocephalus
Trillo-Contreras, J. L., Ramírez‐Lorca, R., Hiraldo-González, L., Sánchez-Gomar, I., Galán‐Cobo, A., Suárez‐Luna, N., Pedro, E. S. D. R.-D., Toledo‐Aral, J. J., Villadiego, J., & Echevarrı́a, M. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.08.006 · Cited by 38 · see citing works
Late-life intermittent fasting decreases aging-related frailty and increases renal hydrogen sulfide production in a sexually dimorphic manner
Henderson, Y. O., Bithi, N., Link, C., Yang, J., Schugar, R. C., Llarena, N. C., Brown, J. M., & Hine, C. (2021) · GeroScience · doi:10.1007/s11357-021-00330-4 · Cited by 38 · see citing works
Traceable Nano‐Biohybrid Complexes by One‐Step Synthesis as CRISPR‐Chem Vectors for Neurodegenerative Diseases Synergistic Treatment
Shen, J., Lü, Z., Wang, J., Hao, Q., Ji, W., Wu, Y., Peng, H., Zhao, R., Yang, J., Li, Y., et al. (2021) · Advanced Materials · doi:10.1002/adma.202101993 · Cited by 38 · see citing works
Cognitive, emotional and social phenotyping of mice in an observer-independent setting
Dere, E., Ronnenberg, A., Tampe, B., Arinrad, S., Schmidt, M., Zeisberg, E. M., & Ehrenreich, H. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.02.023 · Cited by 37 · see citing works
The Period 2 Enhancer Nobiletin as Novel Therapy in Murine Models of Circadian Disruption Resembling Delirium*
Gile, J. J., Scott, B. K., & Eckle, T. D. L. G. (2018) · Critical Care Medicine · doi:10.1097/ccm.0000000000003077 · Cited by 37 · see citing works
Carvacrol ameliorates behavioral disturbances and DNA damage in the brain of rats exposed to propiconazole
Elhady, M. A., Khalaf, A. A. A., Kamel, M. M., & Noshy, P. A. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.10.008 · Cited by 36 · see citing works
“Although, there was no significant difference between all groups in the time spent in exploration of the novel object; the time spent in exploration of the familiar object was significantly higher in PCZ treated rats which is considered as an indicator for cognitive impairment (Wolf et al., 2016).”
Background
Design, synthesis, and evaluation of some novel biphenyl imidazole derivatives for the treatment of Alzheimer's disease
Ramrao, S. P., Verma, A., Waiker, D. K., Tripathi, P. N., & Shrivastava, S. K. (2021) · Journal of Molecular Structure · doi:10.1016/j.molstruc.2021.131152 · Cited by 36 · see citing works
Structure-activity relationship study of tryptophan-based butyrylcholinesterase inhibitors
Meden, A., Knez, D., Malikowska‐Racia, N., Brazzolotto, X., Nachon, F., Svete, J., Sałat, K., Grošelj, U., & Gobec, S. (2020) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2020.112766 · Cited by 34 · see citing works
Repurposing beta-3 adrenergic receptor agonists for Alzheimer’s disease: beneficial effects in a mouse model
Tournissac, M., Vu, T.-M., Vrabic, N., Hozer, C., Tremblay, C., Mélançon, K., Planel, E., Pifferi, F., & Calon, F. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00842-3 · Cited by 33 · see citing works
The Lovebug Effect: Is the human biophilic drive influenced by interactions between the host, the environment, and the microbiome?
Robinson, J. M., & Breed, M. F. (2020) · Science of The Total Environment · doi:10.1016/j.scitotenv.2020.137626 · Cited by 30 · see citing works
A novel molecular class that recruits HDAC/MECP2 complexes to PU.1 motifs reduces neuroinflammation
Ralvenius, W. T., Mungenast, A. E., Woolf, H., Huston, M. M., Gillingham, T. Z., Godin, S. K., Penney, J., Cam, H. P., Gao, F., Fernandez, C. G., et al. (2023) · Journal of Experimental Medicine · doi:10.1084/jem.20222105 · Cited by 31 · see citing works
“CK-p25 mice that were induced (off-Dox) for 6 wk and 1-yr-old P301STau mice underwent the behavioral tasks of open field activity, Y maze, and Morris water maze (Wolf et al., 2016).”
Netrin-1 Ameliorates Postoperative Delirium-Like Behavior in Aged Mice by Suppressing Neuroinflammation and Restoring Impaired Blood-Brain Barrier Permeability
Li, K., Wang, J., Chen, L., Guo, M., Zhou, Y., Li, X., 张宗泽, & Peng, M. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.751570 · Cited by 31 · see citing works
“Mice underwent testing in the Y-maze test to assess spatial learning and memory ability following surgery/anesthesia (Chen et al., 2014; Wolf et al., 2016).”
Method
The Neuropeptide Oxytocin Enhances Information Sharing and Group Decision Making Quality
de Wilde, T. R. W., Velden, F. S. T., & Dreu, C. K. W. D. (2017) · Scientific Reports · doi:10.1038/srep40622 · Cited by 30 · see citing works
LiCl Pretreatment Ameliorates Adolescent Methamphetamine Exposure-Induced Long-Term Alterations in Behavior and Hippocampal Ultrastructure in Adulthood in Mice
Yan, P., Xu, D., Ji, Y., Yin, F., Cui, J., Su, R., Wang, Y., Zhu, Y., Wei, S., & Lai, J. (2019) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyz001 · Cited by 30 · see citing works
“In contrast to previous studies, to increase recognition and navigation in the novel space, we marked the wall of the novel arm with a black and white pattern that was entirely different from the other 2 arms (Dellu et al., 2000; Melnikova et al., 2006; Wolf et al., 2016).”
MethodResult
Adolescent behavioral abnormalities in a Scn1a+/− mouse model of Dravet syndrome
Bahceci, D., Anderson, L. L., Brown, C., Zhou, C., & Arnold, J. C. (2019) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2019.106842 · Cited by 30 · see citing works
Genetic deletion of microRNA-22 blunts the inflammatory transcriptional response to status epilepticus and exacerbates epilepsy in mice
Silva, L. F. A., Reschke, C. R., Nguyen, T. N., Langa, E., Sanz‐Rodriguez, A., Gerbatin, R. R., Temp, F. R., de Freitas, M. L., Conroy, R. M., Brennan, G. P., et al. (2020) · Molecular Brain · doi:10.1186/s13041-020-00653-x · Cited by 28 · see citing works
PERK Regulates Working Memory and Protein Synthesis-Dependent Memory Flexibility
Zhu, S., Henninger, K., McGrath, B. C., & Cavener, D. R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0162766 · Cited by 28 · see citing works
Ebselen inhibits the activity of acetylcholinesterase globular isoform G4 in vitro and attenuates scopolamine‐induced amnesia in mice
Martini, F., Pesarico, A. P., Brüning, C. A., Zeni, G. R., & Nogueira, C. W. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26731 · Cited by 29 · see citing works
Behavioural, metabolic and neurochemical effects of environmental enrichment in high-fat cholesterol-enriched diet-fed mice
de Souza, R. M., de Souza, L., Machado, A. E., Alves, A. C. D. B., Rodrigues, F. S., Aguiar, A. S., Santos, A. R. S., Bem, A. F. D., & Moreira, E. L. G. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.09.022 · Cited by 27 · see citing works
Transcranial Ultrasound Stimulation of Hypothalamus in Aging Mice
Pang, N., Huang, X., Zhou, H., Xia, X., Liu, X., Wang, Y., Meng, W., Bian, T., Meng, L., Xu, L., et al. (2020) · IEEE Transactions on Ultrasonics Ferroelectrics and Frequency Control · doi:10.1109/tuffc.2020.2968479 · Cited by 29 · see citing works
Surgery, Anesthesia and Intensive Care Environment Induce Delirium-Like Behaviors and Impairment of Synaptic Function-Related Gene Expression in Aged Mice
Illendula, M., Osuru, H. P., Ferrarese, B., Atluri, N., Dulko, E., Zuo, Z., & Lunardi, N. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.542421 · Cited by 29 · see citing works
Melatonin Improves Short-Term Spatial Memory in a Mouse Model of Alzheimer’s Disease
Labban, S. Y., Alshehri, F. S., Kurdi, M. E., Alatawi, Y. M., & Alghamdi, B. S. A. (2021) · Degenerative Neurological and Neuromuscular Disease · doi:10.2147/dnnd.s291172 · Cited by 29 · see citing works
“Between each trial, the maze arms were wiped with 70% alcohol to avoid odour cues.(52) The maze arms were labelled A, B, and C.”
Method
Galantamine Nanoparticles Outperform Oral Galantamine in An Alzheimer’S Rat Model: Pharmacokinetics and Pharmacodynamics
El-Ganainy, S. O., Gowayed, M. A., Agami, M. A., Mohamed, P., Belal, M., Farid, R. M., & Hanafy, A. S. (2021) · Nanomedicine · doi:10.2217/nnm-2021-0051 · Cited by 28 · see citing works
Life-span characterization of epilepsy and comorbidities in Dravet syndrome mice carrying a targeted deletion of exon 1 of the Scn1a gene
Gerbatin, R. R., Augusto, J., Boutouil, H., Reschke, C. R., & Henshall, D. C. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114090 · Cited by 29 · see citing works
“Spatial reference, working and recognition memory was assessed with the Y maze and novel object recognition test, respectively (Wolf et al., 2016; Lueptow, 2017).”
Method
Galantamine tethered hydrogel as a novel therapeutic target for streptozotocin-induced Alzheimer’s disease in Wistar rats
Rajkumar, M., Sakthivel, M., Senthilkumar, K., Thangaraj, R., & Kannan, S. (2022) · Current Research in Pharmacology and Drug Discovery · doi:10.1016/j.crphar.2022.100100 · Cited by 29 · see citing works
“However, the Y-maze test based on the transfer latency for food intake showed that memory improvement occurred in the hydrogel-based drug treated rats compared with ICV-STZ induced rats, thereby indicating a greater effect on cognitive improvement (Wolf et al., 2016; Kitanaka et al., 2015).”
Method
Bile duct ligation of C57BL/6 mice as a model of hepatic encephalopathy
Cho, I., Koo, B., Kam, E. H., Lee, S. K., Oh, H., & Kim, S. Y. (2020) · Anesthesia and Pain Medicine · doi:10.17085/apm.2020.15.1.19 · Cited by 28 · see citing works
“After 1 h, one of the familiar objects was replaced with a novel object and free exploration was allowed for 10 min [17].”
Background
Impact of different fructose concentrations on metabolic and behavioral parameters of male and female mice
Souza, L. D., Barros, W. D. M., de Souza, R. M., Delanogare, E., Machado, A. E., Braga, S. P., Rosa, G. K., Nardi, G. M., Rafacho, A., Speretta, G. F. F., et al. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113187 · Cited by 28 · see citing works
Doxycycline reverses cognitive impairment, neuroinflammation and oxidative imbalance induced by D-amphetamine mania model in mice: A promising drug repurposing for bipolar disorder treatment?
Filho, A. J. M. C., Cunha, N. L., Rodrigues, P. D. A., de Souza, A. G., Soares, M. V.-R., Jucá, P. M., de Queiroz, T., Clemente, D. C. D. S., Mottin, M., Andrade, C. H., et al. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2020.11.007 · Cited by 28 · see citing works
Rhythmic air-puff into nasal cavity modulates activity across multiple brain areas: A non-invasive brain stimulation method to reduce ventilator-induced memory impairment
Ghazvineh, S., Salimi, M., Nazari, M., Garousi, M., Tabasi, F., Dehdar, K., Salimi, A., Jamaati, H., Mirnajafi‐Zadeh, J., Arabzadeh, E., et al. (2021) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2021.103627 · Cited by 27 · see citing works
Sevoflurane Improves Hemorrhagic Shock and Resuscitation‐Induced Cognitive Impairments and Mitochondrial Dysfunctions through SIRT1‐Mediated Autophagy
Shu, J., Huang, X., Liao, Q., Wang, J., Zhou, Y., Chen, Y., Chen, M., Qian, C., Zhang, Y., Hu, X., et al. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/9771743 · Cited by 27 · see citing works
“During the test phase, the mouse was returned to the arena with two di ﬀ erent objects: one is identical to the old and the other one is novel (A+B) [23].”
Behavioral analysis of motor and non-motor impairment in rodent models of Parkinson's disease
Sheta, R., Bérard, M., Musiol, D., Martínez-Drudis, L., & Oueslati, A. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1464706 · Cited by 29 · see citing works
Effects of Hippeastrum reticulatum on memory, spatial learning and object recognition in a scopolamine-induced animal model of Alzheimer’s disease
Hoang, T. H. X., Hồ, Đ. V., Phan, K. V., Le, Q. V., Raal, A., & Nguyen, H. T. (2020) · Pharmaceutical Biology · doi:10.1080/13880209.2020.1841810 · Cited by 27 · see citing works
“The Y-maze test, Morris water-maze test and recognition tests are usually applied in previous studies (Wolf et al. 2016; Lueptow 2017; Kraeuter et al. 2019).”
BackgroundMethod
Ellagic Acid Modulates the Amyloid Precursor Protein Gene via Superoxide Dismutase Regulation in the Entorhinal Cortex in an Experimental Alzheimer’s Model
Ramadan, W. S., & Alkarim, S. (2021) · Cells · doi:10.3390/cells10123511 · Cited by 26 · see citing works
“Behavioral tests, such as the Y-maze test, Morris water-maze test, and NORT, have been used to study memory [37–39].”
The Antidepressant and Cognitive Improvement Activities of the Traditional Chinese Herb Cistanche
Wang, D., Wang, H., & Gu, L. (2017) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2017/3925903 · Cited by 26 · see citing works
Age-Dependent Alterations of Cognition, Mitochondrial Function, and Beta-Amyloid Deposition in a Murine Model of Alzheimer’s Disease—A Longitudinal Study
Reutzel, M., Grewal, R., Joppe, A., & Eckert, G. P. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.875989 · Cited by 25 · see citing works
“The Y-Maze test provides insight into motor skills and spatial learning memory (Wolf et al., 2016).”
Method
Potential Mechanisms of Imidacloprid-Induced Neurotoxicity in Adult Rats with Attempts on Protection Using Origanum majorana L. Oil/Extract: In Vivo and In Silico Studies
Hassanen, E. I., Issa, M. Y., Hassan, N. H., Ibrahim, M. A., Fawzy, I. M., Fahmy, S. A., & Mehanna, S. (2023) · ACS Omega · doi:10.1021/acsomega.2c08295 · Cited by 25 · see citing works
A fully automated home cage for long-term continuous phenotyping of mouse cognition and behavior
Ho, H., Kejzar, N., Sasaguri, H., Saito, T., Saido, T. C., Strooper, B. D., Bauža, M., & Krupic, J. (2023) · Cell Reports Methods · doi:10.1016/j.crmeth.2023.100532 · Cited by 26 · see citing works
“These tasks constitute some of the most widely used spatial memory tasks and are part of most standard behavioral test batteries designed to assess learning and memory.(18) In addition, the system monitors an animal’s position, water consumption, quiescence, and locomotion patterns.”
Background
Altered dietary selenium influences brain iron content and behavioural outcomes
Sharma, S. K., Bansal, M. P., & Sandhir, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112011 · Cited by 25 · see citing works
Development and Evaluation of Some Molecular Hybrids of N-(1-Benzylpiperidin-4-yl)-2-((5-phenyl-1,3,4-oxadiazol-2-yl)thio) as Multifunctional Agents to Combat Alzheimer’s Disease
Waiker, D. K., Verma, A., Saraf, P., Gajendra, T. A., Krishnamurthy, S., Chaurasia, R. N., & Shrivastava, S. K. (2023) · ACS Omega · doi:10.1021/acsomega.2c08061 · Cited by 25 · see citing works
Design, Synthesis, and Biological Investigation of Quinazoline Derivatives as Multitargeting Therapeutics in Alzheimer’s Disease Therapy
Verma, A., Waiker, D. K., Singh, N. D., Roy, A., Singh, N., Saraf, P., Bhardwaj, B., Krishnamurthy, S., Trigun, S. K., & Shrivastava, S. K. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00653 · Cited by 24 · see citing works
Effects of Long-Term Rice Bran Extract Supplementation on Survival, Cognition and Brain Mitochondrial Function in Aged NMRI Mice
Hagl, S., Asseburg, H., Heinrich, M., Sus, N., Blumrich, E., Dringen, R., Frank, J., & Eckert, G. P. (2016) · NeuroMolecular Medicine · doi:10.1007/s12017-016-8420-z · Cited by 24 · see citing works
Space fit for a king: spatial ecology of king cobras (Ophiophagus hannah) in Sakaerat Biosphere Reserve, Northeastern Thailand
Marshall, B. M., Strine, C. T., Jones, M. D., Artchawakom, T., Silva, I., Suwanwaree, P., & Goode, M. (2018) · Amphibia-Reptilia · doi:10.1163/15685381-18000008 · Cited by 24 · see citing works

P1–081: Learning and memory changes in Tg2576 transgenic mice: A longitudinal study
Laszy, J., Gyertyán, I., Boros, A. M., Urbányi, Z., Dezsło, P., & Szendrei, G. I. (2006) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2006.05.456
APP-Based Transgenic Models: The Tg2576 Model
Deacon, R. M. J. (2010) · Neuromethods · doi:10.1007/978-1-60761-898-0_19 · Cited by 3 · see citing works
Mice expressing the Swedish APP mutation on a 129 genetic background demonstrate consistent behavioral deficits and pathological markers of Alzheimer's disease
Rustay, N. R., Cronin, E. A., Curzon, P., Markosyan, S., Bitner, R. S., Ellis, T. A., Waring, J. F., Decker, M. W., Rueter, L. E., & Browman, K. E. (2009) · Brain Research · doi:10.1016/j.brainres.2009.11.040 · Cited by 38 · see citing works
P1‐027: BEHAVIORAL CHARACTERIZATION OF TG2576 MICE IN TOUCHSCREEN TASKS TARGETING DIFFERENT ASPECTS OF LEARNING AND MEMORY
Dorner‐Ciossek, C., Delotterie, D. F., Mathis, C., Cassel, J., Rosenbrock, H., & Marti, A. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2014.05.262
Early impairment in a water-finding test in a longitudinal study of the Tg2576 mouse model of Alzheimer's disease
Kishimoto, Y., Higashihara, E., Fukuta, A., Nagao, A., & Kirino, Y. (2012) · Brain Research · doi:10.1016/j.brainres.2012.10.066 · Cited by 21 · see citing works

Authors: Wolf, A., Bauer, B., Abner, E. L., Ashkenazy-Frolinger, T., & Hartz, A. M. S.
Affiliations: University of Minnesota, Duluth (US)
University of Kentucky (US)
Corresponding author: Hartz, Anika M. S.
ORCID: Bauer, Björn
Abner, Erin L.
Hartz, Anika M. S.
Venue: PLOS ONE
Publisher: Public Library of Science (PLoS)
Published: 2016-01-25
Volume: 11
Issue: 1
Pages: e0147733
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0147733
PMC: PMC4726499
OpenAlex: W2426168356
Cited by: 281
References: 89
Citations by year: 2026: 16 · 2025: 20 · 2024: 28 · 2023: 37 · 2022: 30 · 2021: 33 · 2020: 37 · 2019: 28 · 2018: 40 · 2017: 6 · 2016: 6
FWCI: 21.46
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
UKnowledge (University of Kentucky) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: University of Kentucky (P30 AG028383, AG028383)
National Institute on Aging (AG-028383, P30AG028383, R01AG039621)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Keywords: mouse models of Alzheimer's disease, amyloid precursor protein overexpression, retinal degeneration, scopolamine-induced dementia, cognitive impairment, learning and memory, novel object recognition, Morris water maze, radial arm water maze, spontaneous alternation, amyloid-beta pathology
MeSH terms: Animals, Behavior, Animal, Male, Memory, Mice, Transgenic, Maze Learning, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

A Comprehensive Behavioral Test Battery to Assess Learning and Memory in 129S6/Tg2576 Mice

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks