A combined marble burying–locomotor activity test in mice: A practical screening test with sensitivity to different classes of anxiolytics and antidepressants
Abstract
Over the last decades, the inhibition of spontaneous burying of glass marbles by mice has been used as an index of anxiolytic drug action in the so-called marble burying test. Indeed, acute administration of rapid-onset (e.g. diazepam) and slow-onset (e.g. fluoxetine) anxiolytics inhibit marble burying. However, non-anxiolytic compounds such as classical antipsychotics also reduce marble burying thus suggesting that the predictive validity of this procedure for anxiety may be limited. In the present study, after having selected a strain of mice (C57BL/6J) that showed spontaneous avoidance of glass marbles, we tried to improve the predictive validity of the marble burying test for anxiety by measuring locomotor activity during the marble burying test and--if needed--in control experiments by using a videotracking system. Twenty-four reference compounds were tested including anxiolytics, anxiogenics, antidepressants, antipsychotics and other classes. By comparing marble burying scores with locomotor measures, we found that, based on our criteria, most of the anxiolytics and antidepressants selectively inhibited marble burying in contrast to most of the other compounds (e.g. haloperidol, morphine). Two putative anxiolytics, i.e. the nociceptin orphanin FQ peptide receptor agonist Ro 64-6198 and the metabotropic glutamate 5 receptor antagonist 2-methyl-6-(phenylethynyl)pyridine, also showed a selective profile. We propose this modified procedure, requiring only a limited number of animals, as a valuable screening test for the detection of compounds having anxiolytic effects.
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The marble-burying test is a rodent model of anxiety that has high predictive value to detect anxiolytic-like activity of acutely administered drugs.
“The marble-burying test is a rodent model of anxiety that has high predictive value to detect anxiolytic-like activity of acutely administered drugs (Nicolas et al, 2006).”
From Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal (2013) · cites this paper as Nicolas et al, 2006
The marble-burying test strongly predicts anxiolytic-like activity of drugs given acutely.
“This test has high predictive value to detect anxiolytic-like activity of acutely administered drugs (Nicolas et al., 2006), which is demonstrated by the positive result of CDP (10 mg/kg) in this test (Fig. 2).”
From Nicotinic Partial Agonists Varenicline and Sazetidine-A Have Differential Effects on Affective Behavior (2010) · cites this paper as Nicolas et al., 2006
Burying behavior is quantifiable and sensitive to anxiolytics.
“This burying behavior is quantifiable and sensitive to anxiolytics45,46.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [45]
Cites
The Neuropsychology of Anxiety
Gray, J. A., & McNaughton, N. (2003) · doi:10.1093/acprof:oso/9780198522713.001.0001 · Cited by 1,933 · see citing works
Bandelow, B., Zohar, J., Hollander, E., Kasper, S., Möller, H., & WFSBP Task Force on Treatment Guide (2008) · The World Journal of Biological Psychiatry · doi:10.1080/15622970802465807 · Cited by 862 · see citing works
Evaluation of marble-burying behavior as a model of anxiety
Njung'e, K., & Handley, S. L. (1991) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(91)90590-x · Cited by 487 · see citing works
The neuropsychology of anxiety
LADER, M. H. (1983) · Personality and Individual Differences · doi:10.1016/0191-8869(83)90137-x · Cited by 418 · see citing works
Defensive burying in rodents: ethology, neurobiology and psychopharmacology
de Boer, S. F., & Koolhaas, J. M. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01278-0 · Cited by 391 · see citing works
Do animal models of anxiety predict anxiolytic-like effects of antidepressants?
Borsini, F., Podhorna, J., & Marazziti, D. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1155-6 · Cited by 347 · see citing works
5-HT2C Receptor Agonists: Pharmacological Characteristics and Therapeutic Potential
Martin, J. R., Bös, M., Jenck, F., Moreau, J., Mutel, V., Sleight, A. J., Wichmann, J., Andrews, J. S., Berendsen, H. H. G., Broekkamp, C. L. E., et al. (1998) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37669-4 · Cited by 335 · see citing works
Lauria-Horner, B., & Pohl, R. B. (2003) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.12.4.663 · Cited by 327 · see citing works
Porter, R. H. P., Jaeschke, G., Spooren, W., Ballard, T. M., Büttelmann, B., Kolczewski, S., Peters, J.-U., Prinssen, E., Wichmann, J., Vieira, E., et al. (2005) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.089839 · Cited by 308 · see citing works
Self-citationBroekkamp, C. L., Rijk, H. W., Joly-Gelouin, D., & Lloyd, K. L. (1986) · European Journal of Pharmacology · doi:10.1016/0014-2999(86)90051-8 · Cited by 286 · see citing works
A synthetic agonist at the orphanin FQ/nociceptin receptor ORL1: Anxiolytic profile in the rat
Jenck, F., Wichmann, J., Dautzenberg, F. M., Moreau, J., Ouagazzal, A., Martin, J. R., Lundstrom, K. H., Cesura, A. M., Poli, S. M., Roever, S., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.090514397 · Cited by 275 · see citing works
Spooren, W. P. J. M., Vassout, A., Neijt, H. C., Kuhn, R., Gasparini, F., Roux, S., Porsolt, R. D., & Gentsch, C. (2000) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39029-9 · Cited by 266 · see citing works
Pinna, G., Dong, E., Matsumoto, K., Costa, E., & Guidotti, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337642100 · Cited by 224 · see citing works
On serotonin and experimental anxiety
Graeff, F. G. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1112-4 · Cited by 219 · see citing works
Stahl, S. M. (2004) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v65n0401 · Cited by 204 · see citing works
Njung'e, K., & Handley, S. L. (1991) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1991.tb12392.x · Cited by 183 · see citing works
Guidotti, A., Dong, E., Matsumoto, K., Pinna, G., Rasmusson, A. M., & Costa, E. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00129-1 · Cited by 169 · see citing works
Bandelow, B., Zohar, J., Hollander, E., Kasper, S. F., Möller, H., & WFSBP Task Force on Treatment Guide (2002) · The World Journal of Biological Psychiatry · doi:10.3109/15622970209150621 · Cited by 167 · see citing works
Ichimaru, Y., Egawa, T., & Sawa, A. (1995) · Japanese Journal of Pharmacology · doi:10.1254/jjp.68.65 · Cited by 163 · see citing works
Busse, C. S., Brodkin, J. D., Tattersall, D., Anderson, J. J., Warren, N., Tehrani, L. R., Bristow, L. J., Varney, M. A., & Cosford, N. D. P. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300540 · Cited by 159 · see citing works
Pregabalin may represent a novel class of anxiolytic agents with a broad spectrum of activity
Field, M. J., Oles, R. J., & Singh, L. (2001) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703794 · Cited by 129 · see citing works
(1995) · doi:10.1097/00008877-199505001-00026 · Cited by 119 · see citing works
Millan, M. J., Dekeyne, A., Papp, M., Rochelle, C. D. L., MacSweeny, C., Péglion, J.-L., & Brocco, M. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29416-7 · Cited by 117 · see citing works
Investigative burying by laboratory mice may involve non-functional, compulsive, behaviour
Londei, T., Valentini, A. M. V., & Leone, V. G. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00162-9 · Cited by 110 · see citing works
BURYING BY RATS IN RESPONSE TO AVERSIVE AND NONAVERSIVE STIMULI
Poling, A. D., Cleary, J. P., & Monaghan, M. M. (1981) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1981.35-31 · Cited by 94 · see citing works
A comparison of anxiolytic and nonanxiolytic agents in the shock-probe/burying test for anxiolytics
Treit, D. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90151-7 · Cited by 86 · see citing works
RAT DEFENSIVE BEHAVIOR: BURYING NOXIOUS FOOD1
Wilkie, D. M., MacLennan, A. J., & Pinel, J. P. J. (1979) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1979.31-299 · Cited by 82 · see citing works
Imidazenil and diazepam increase locomotor activity in mice exposed to protracted social isolation
Pinna, G., Agís‐Balboa, R. C., Zhubi, A., Matsumoto, K., Grayson, D. R., Costa, E., & Guidotti, A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600329103 · Cited by 79 · see citing works
Jenck, F., Moreau, J., Berendsen, H. H. G., Boes, M., Broekkamp, C. L. E., Martin, J. R., Wichmann, J., & Delft, A. M. L. V. (1998) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(97)00055-2 · Cited by 68 · see citing works
Welch, B. L., & Welch, A. S. (1968) · Journal of Pharmacy and Pharmacology · doi:10.1111/j.2042-7158.1968.tb09734.x · Cited by 66 · see citing works
Involvement of adrenergic and cholinergic systems in nicotine-induced anxiogenesis in mice
Zarrindast, M., Homayoun, H., Babaie, A., Etminani, A., & Gharib, B. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00628-2 · Cited by 60 · see citing works
ARCHER, T., FREDRIKSSON, A., LEWANDER, T., & SÖDERBERG, U. (1987) · Scandinavian Journal of Psychology · doi:10.1111/j.1467-9450.1987.tb00761.x · Cited by 58 · see citing works
Effects of scopolamine and its quaternary analogue in the murine elevated plus-maze test of anxiety
Rodgers, R. J., & Cole, J. C. (1995) · Behavioural Pharmacology · doi:10.1097/00008877-199504000-00009 · Cited by 52 · see citing works
Rilke, O., Freier, D., Jähkel, M., & Oehler, J. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00509-1 · Cited by 51 · see citing works
Millan, M. J., Girardon, S., Mullot, J., Brocco, M., & Dekeyne, A. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00021-7 · Cited by 46 · see citing works
Söderpalm, B., Eriksson, E., & Engel, J. A. (1989) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(89)90024-9 · Cited by 43 · see citing works
Scopolamine: Effects on fear or defense responses in the rat
Mollenauer, S. O., Plotnik, R., & Southwick, P. C. (1976) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(76)90032-0 · Cited by 9 · see citing works
Gray, J. A., & McNaughton, N. (2003) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198522713.003.0002 · Cited by 7 · see citing works
Clinical and metabolic responses to different kinds of premedication in ASA III patients
Kirvela, O. A., & Kanto, J. (1992) · Acta Anaesthesiologica Scandinavica · doi:10.1111/j.1399-6576.1992.tb03564.x · Cited by 3 · see citing works
P.4.036 The marble burying test in mice: can its predictive validity for anxiety be improved?
(2005) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(05)81135-6 · Cited by 1 · see citing works
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1 of the 41 references couldn’t be matched to a known paper.
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Sorted by citations
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety
Thomas, A., Burant, A., Bui, N., Graham, D., Yuva-Paylor, L. A., & Paylor, R. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1466-y · Cited by 698 · see citing works
Deiana, S., Watanabe, A., Yamasaki, Y., Amada, N., Arthur, M., Fleming, S., Woodcock, H., Dorward, P. K., Pigliacampo, B., Close, S., et al. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2415-0 · Cited by 399 · see citing works
Toll, L., Bruchas, M. R., Calò, G., Cox, B. M., & Zaveri, N. T. (2016) · Pharmacological Reviews · doi:10.1124/pr.114.009209 · Cited by 301 · see citing works
Savelieva, K. V., Zhao, S., Pogorelov, V. M., Rajan, I., Yang, Q., Cullinan, E. B., & Lanthorn, T. H. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003301 · Cited by 265 · see citing works
Marks, D. R., Tucker, K., Cavallin, M. A., Mast, T. G., & Fadool, D. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1350-09.2009 · Cited by 242 · see citing works
The 5-HT7 receptor and disorders of the nervous system: an overview
Hedlund, P. B. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1626-0 · Cited by 239 · see citing works
A Time-Dependent History of Mood Disorders in a Murine Model of Neuropathic Pain
Yalçın, İ., Bohren, Y., Waltisperger, E., Ciocca, D., Yin, J. C. P., Freund‐Mercier, M. J., & Barrot, M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.017 · Cited by 233 · see citing works
de Brouwer, G., Fick, A., Harvey, B. H., & Wolmarans, D. W. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-00653-4 · Cited by 188 · see citing works
Pentkowski, N. S., Rogge-Obando, K., Donaldson, T. N., Bouquin, S. J., & Clark, B. J. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.05.005 · Cited by 169 · see citing works
Chioca, L. R., Ferro, M. M., Baretta, I. P., Oliveira, S. M., Silva, C. R., Ferreira, J., Losso, E. M., & Andreatini, R. (2013) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2013.03.028 · Cited by 167 · see citing works
Human-Derived Bifidobacterium dentium Modulates the Mammalian Serotonergic System and Gut–Brain Axis
Engevik, M. A., Luck, B., Visuthranukul, C., Ihekweazu, F. D., Engevik, A. C., Shi, Z., Danhof, H. A., Chang-Graham, A. L., Hall, A., Endres, B. T., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.08.002 · Cited by 164 · see citing works
Sciatic nerve cuffing in mice: A model of sustained neuropathic pain
Benbouzid, M., Pallage, V., Rajalu, M., Waltisperger, E., Doridot, S., Poisbeau, P., Freund‐Mercier, M. J., & Barrot, M. (2007) · European Journal of Pain · doi:10.1016/j.ejpain.2007.10.002 · Cited by 164 · see citing works
Role of the 5-HT7 Receptor in the Central Nervous System: from Current Status to Future Perspectives
Matthys, A., Haegeman, G., van Craenenbroeck, K., & Vanhoenacker, P. (2011) · Molecular Neurobiology · doi:10.1007/s12035-011-8175-3 · Cited by 163 · see citing works
Rose, J. H., Karkhanis, A. N., Chen, R., Gioia, D., Lopez, M. F., Becker, H. C., McCool, B. A., & Jones, S. R. (2016) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv127 · Cited by 136 · see citing works
Dekeyne, A., la Cour, C. M., Gobert, A., Brocco, M., Lejeune, F., Serres, F., Sharp, T., Daszuta, A., Soumier, A., Papp, M., et al. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1177-9 · Cited by 126 · see citing works
Ortuño, M. J., Robinson, S. T., Subramanyam, P., Paone, R., Huang, Y.-Y., Guo, X.-D. E., Colecraft, H. M., Mann, J. J., & Ducy, P. F. (2016) · Nature Medicine · doi:10.1038/nm.4166 · Cited by 111 · see citing works
Barnum, C. J., Pace, T. W., Hu, F., Neigh, G. N., & Tansey, M. G. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-9 · Cited by 107 · see citing works
Adeluyi, A., Guerin, L. N., Fisher, M. L., Galloway, A. L., Cole, R. D., Chan, S. S. L., Wyatt, M. D., Davis, S. W., Freeman, L. R., Ortinski, P. I., et al. (2019) · Science Advances · doi:10.1126/sciadv.aax7031 · Cited by 107 · see citing works
Marble burying as a test of the delayed anxiogenic effects of acute immobilisation stress in mice
Kedia, S., & Chattarji, S. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.06.012 · Cited by 101 · see citing works
Kalinichev, M., Rouillier, M., Girard, F., Royer-Urios, I., Bournique, B., Finn, T., Charvin, D., Campo, B., Poul, E. L., Mutel, V., et al. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.200915 · Cited by 101 · see citing works
Involvement of endocannabinoids in antidepressant and anti-compulsive effect of fluoxetine in mice
Umathe, S. N., Manna, S. S. S., & Jain, N. S. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.031 · Cited by 96 · see citing works
Egashira, N., Okuno, R., Harada, S., Matsushita, M., Mishima, K., Iwasaki, K., Nishimura, R., Oishi, R., & Fujiwara, M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.01.035 · Cited by 95 · see citing works
Endogenous opiates and behavior: 2006
Bodnar, R. J. (2007) · Peptides · doi:10.1016/j.peptides.2007.09.002 · Cited by 91 · see citing works
de Almeida, A. A. C., de Carvalho, R. B. F., Silva, O. A., de Sousa, D. P., & de Freitas, R. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.01.006 · Cited by 90 · see citing works
Turner, J. R., Castellano, L. M., & Blendy, J. A. (2010) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.166280 · Cited by 88 · see citing works
Behavioral Disinhibition and Reduced Anxiety-like Behaviors in Monoamine Oxidase B-Deficient Mice
Bortolato, M., Godar, S. C., Davarian, S., Chen, K., & Shih, J. C. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.118 · Cited by 90 · see citing works
Millan, M. J. (2010) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2010.06.002 · Cited by 91 · see citing works
Zike, I. D., Xu, T., Hong, N., & Veenstra-VanderWeele, J. M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.09.012 · Cited by 82 · see citing works
The 5-HT7 receptor influences stereotypic behavior in a model of obsessive-compulsive disorder
Hedlund, P. B., & Sutcliffe, J. G. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2006.12.054 · Cited by 84 · see citing works
Turner, J. R., Castellano, L. M., & Blendy, J. A. (2011) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntq206 · Cited by 78 · see citing works
Varty, G. B., Lu, S. X., Morgan, C. A., Cohen-Williams, M. E., Hodgson, R. A., Smith‐Torhan, A., Zhang, H., Fawzi, A. B., Graziano, M. P., Ho, G. D., et al. (2008) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.136937 · Cited by 81 · see citing works
Marble-burying behavior test as a murine model of compulsive-like behavior
Dixit, P. V., Sahu, R. A., & Mishra, D. K. (2020) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2020.106676 · Cited by 77 · see citing works
Huang, G.-J., Bannerman, D. M., & Jonathan Flint, C. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002104 · Cited by 77 · see citing works
Animal Models of Anxiety and Anxiolytic Drug Action
Treit, D., Engin, E., & McEown, K. (2009) · Current topics in behavioral neurosciences · doi:10.1007/7854_2009_17 · Cited by 77 · see citing works
mGlu5negative allosteric modulators: a patent review (2013 - 2016)
Emmitte, K. A. (2017) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2017.1280466 · Cited by 76 · see citing works
“Bedside-to-Bench” Behavioral Outcomes in Animal Models of Pain: Beyond the Evaluation of Reflexes
Cobos, E. J., & Portillo-Salido, E. F. (2013) · Current Neuropharmacology · doi:10.2174/1570159x113119990041 · Cited by 74 · see citing works
Anxiolytic-like effects of acute and chronic treatment with Achillea millefolium L. extract
Baretta, I. P., Felizardo, R. A., Bimbato, V. F., dos Santos, M. G. J., Kassuya, C. A. L., Gasparotto, A., da Silva, C. R., Oliveira, S. M., Ferreira, J., & Andreatini, R. (2011) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2011.11.047 · Cited by 74 · see citing works
Experimental Models of Anxiety for Drug Discovery and Brain Research
Hart, P. C., Bergner, C., Smolinsky, A. N., Dufour, B. D., Egan, R. J., LaPorte, J. L., & Kalueff, A. V. (2009) · Methods in molecular biology · doi:10.1007/978-1-60761-058-8_18 · Cited by 74 · see citing works
Marble burying as compulsive behaviors in male and female mice
Taylor, G. T., Lerch, S., & Chourbaji, S. (2017) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2017-059 · Cited by 74 · see citing works
Tasan, R. O., Lin, S., Hetzenauer, A., Singewald, N., Herzog, H., & Sperk, G. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2008.11.048 · Cited by 71 · see citing works
“…Lecci et al., 1990; Olivier et al., 2003; Van der Heyden et al., 1997) and the marble burying test (Borsini et al., 2002; Broekkamp et al., 1986; Nicolas et al., 2006; Njung’e and Handley, 1991; Xu et al., 2004), that are independent or even inversely dependent on motor activity, respectively.”
BackgroundRecent Advances in the Design and Development of Novel Negative Allosteric Modulators of mGlu5
Emmitte, K. A. (2011) · ACS Chemical Neuroscience · doi:10.1021/cn2000266 · Cited by 70 · see citing works
Down Syndrome Cognitive Phenotypes Modeled in Mice Trisomic for All HSA 21 Homologues
Belichenko, P. V., Kleschevnikov, A. M., Becker, A., Wagner, G. E., Lysenko, L. V., Yu, Y. E., & Mobley, W. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134861 · Cited by 70 · see citing works
Kalinichev, M., Poul, E. L., Boléa, C., Girard, F., Campo, B., Fonsi, M., Royer-Urios, I., Browne, S. E., Uslaner, J. M., Davis, M. J., et al. (2014) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.214437 · Cited by 70 · see citing works
Bespalov, A., van Gaalen, M. M., Sukhotina, I. A., Wicke, K. M., Mezler, M., Schoemaker, H., & Groß, G. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.06.089 · Cited by 68 · see citing works
Engers, J. L., Rodriguez, A. L., Konkol, L. C., Morrison, R. D., Thompson, A. D., Byers, F. W., Blobaum, A. L., Chang, S., Venable, D. F., Loch, M. T., et al. (2015) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.5b01005 · Cited by 66 · see citing works
Winocur, G., Johnston, I., & Castel, H. (2018) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2018.05.017 · Cited by 60 · see citing works
Fedotova, J., Kubatka, P., Büsselberg, D., Shleikin, A. G., Caprnda, M., Dragasek, J., Rodrigo, L., Pohanka, M., Gasparova, I., Nosal, V., et al. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.08.107 · Cited by 59 · see citing works
mGlu5negative allosteric modulators: a patent review (2010 – 2012)
Emmitte, K. A. (2013) · Expert Opinion on Therapeutic Patents · doi:10.1517/13543776.2013.760544 · Cited by 59 · see citing works
Altered anxiety-related behavior in nociceptin/orphanin FQ receptor gene knockout mice
Gavioli, E. C., Rizzi, A., Marzola, G., Zucchini, S., Regoli, D. C., & Calò, G. (2007) · Peptides · doi:10.1016/j.peptides.2007.04.012 · Cited by 58 · see citing works
Odland, A. U., Kristensen, J. L., & Andreasen, J. T. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113093 · Cited by 57 · see citing works
Nichols, J. N., Deshane, A. S., Niedzielko, T. L., Smith, C. D., & Floyd, C. L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.10.052 · Cited by 57 · see citing works
Delotterie, D. F., Ruiz, G. T., Brocard, J., Schweitzer, A., Roucard, C., Roche, Y., Suaud‐Chagny, M., Bressand, K., & Andrieux, A. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1712-3 · Cited by 56 · see citing works
Wolmarans, D. W., Stein, D. J., & Harvey, B. H. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0413-8 · Cited by 55 · see citing works
Anosmia does not impair the anxiolytic-like effect of lavender essential oil inhalation in mice
Chioca, L. R., Antunes, V. D., Ferro, M. M., Losso, E. M., & Andreatini, R. (2013) · Life Sciences · doi:10.1016/j.lfs.2013.03.012 · Cited by 55 · see citing works
Reiss, D. J., Wichmann, J., Tekeshima, H., Kieffer, B. L., & Ouagazzal, A. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.10.031 · Cited by 55 · see citing works
Anxiolytic-like effects of carvacryl acetate, a derivative of carvacrol, in mice
Pires, L. F., Costa, L. M., Silva, O. A., de Almeida, A. A. C., Cerqueira, G. S., de Sousa, D. P., & de Freitas, R. M. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.09.001 · Cited by 54 · see citing works
Diazepam causes sedative rather than anxiolytic effects in C57BL/6J mice
Pádua-Reis, M., Nôga, D. A., Tort, A. B. L., & Blunder, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-88599-5 · Cited by 53 · see citing works
Shoblock, J. R. (2007) · CNS Drug Reviews · doi:10.1111/j.1527-3458.2007.00007.x · Cited by 52 · see citing works
Memory Impairment and Reduced Exploratory Behavior in Mice after Administration of Systemic Morphine
Kitanaka, J., Kitanaka, N., Hall, F. S., Fujii, M., Goto, A., Kanda, Y., Koizumi, A., Kuroiwa, H., Mibayashi, S., Muranishi, Y., et al. (2015) · Journal of Experimental Neuroscience · doi:10.4137/jen.s25057 · Cited by 49 · see citing works
The Orphanin FQ/Nociceptin (OFQ/N) System
Civelli, O. (2008) · Springer eBooks · doi:10.1007/400_2007_057 · Cited by 49 · see citing works
Monoamine reuptake inhibition and mood-enhancing potential of a specified oregano extract
Mechan, A. O., Fowler, A. S., Seifert, N., Rieger, H., Woehrle, T., Etheve, S., Wyss, A., Schüler, G., Colletto, B., Kilpert, C., et al. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510004940 · Cited by 47 · see citing works
Evidence from mouse and man for a role of neuregulin 3 in nicotine dependence
Turner, J. R., Ray, R., Lee, B., Everett, L. J., Xiang, J. J., Jepson, C., Kaestner, K. H., Lerman, C. E., & Blendy, J. A. (2013) · Molecular Psychiatry · doi:10.1038/mp.2013.104 · Cited by 46 · see citing works
Heydendael, W., & Jacobson, L. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07131.x · Cited by 44 · see citing works
Mueller, R., Dawson, E. S., Meiler, J., Rodriguez, A. L., Chauder, B. A., Bates, B. S., Felts, A. S., Lamb, J. P., Menon, U. N., Jadhav, S. B., et al. (2012) · ChemMedChem · doi:10.1002/cmdc.201100510 · Cited by 45 · see citing works
Role of Nociceptin/Orphanin FQ-NOP Receptor System in the Regulation of Stress-Related Disorders
Ubaldi, M., Cannella, N., Borruto, A. M., Petrella, M., Bonaventura, M. V. M. D., Soverchia, L., Stopponi, S., Weiss, F., Cifani, C., & Ciccocioppo, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312956 · Cited by 43 · see citing works
Burgado, J., Harrell, C. S., Eacret, D., Reddy, R., Barnum, C. J., Tansey, M. G., Miller, A. H., Wang, H., & Neigh, G. N. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.060 · Cited by 42 · see citing works
Chronic pain causes a persistent anxiety state leading to increased ethanol intake in CD1 mice
González-Sepúlveda, M., Pozo, O. J., Marcos, J., & Valverde, O. (2016) · Journal of Psychopharmacology · doi:10.1177/0269881115622238 · Cited by 40 · see citing works
Umathe, S. N., Vaghasiya, J. M., Jain, N. S., & Dixit, P. V. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.06.013 · Cited by 40 · see citing works
Anderson, S. M., & Brunzell, D. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048665 · Cited by 40 · see citing works
Grados, M. A., Atkins, E., Kovacikova, G. I., & McVicar, E. L. (2015) · Psychology Research and Behavior Management · doi:10.2147/prbm.s58601 · Cited by 39 · see citing works
Neuronal nicotinic receptor antagonist reduces anxiety-like behavior in mice
Roni, M. A., & Rahman, S. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.09.035 · Cited by 35 · see citing works
Odland, A. U., Jessen, L., Kristensen, J. L., Fitzpatrick, C. M., & Andreasen, J. T. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107838 · Cited by 35 · see citing works
Suryanto, M. E., Audira, G., Uapipatanakul, B., Hussain, A., Saputra, F., Siregar, P., Chen, K. H. ‐., & Hsiao, C. (2021) · Cells · doi:10.3390/cells10040738 · Cited by 35 · see citing works
Nickols, H. H., Yuh, J. P., Gregory, K. J., Morrison, R. D., Bates, B. S., Stauffer, S. R., Emmitte, K. A., Bubser, M., Peng, W., Nedelcovych, M. T., et al. (2015) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.115.226597 · Cited by 34 · see citing works
Vincenzi, F., Ravani, A., Pasquini, S., Merighi, S., Gessi, S., Romagnoli, R., Baraldi, P. G., Borea, P. A., & Varani, K. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.09.015 · Cited by 34 · see citing works
Felts, A. S., Rodriguez, A. L., Blobaum, A. L., Morrison, R. D., Bates, B. S., Gray, A. T., Rook, J. M., Tantawy, M. N., Byers, F. W., Chang, S., et al. (2017) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.7b00410 · Cited by 34 · see citing works
NrCAM ‐regulating neural systems and addiction‐related behaviors
Ishiguro, H., Hall, F. S., Horiuchi, Y., Sakurai, T., Hishimoto, A., Grumet, M., Uhl, G. R., Onaivi, E. S., & Arinami, T. (2012) · Addiction Biology · doi:10.1111/j.1369-1600.2012.00469.x · Cited by 34 · see citing works
Felts, A. S., Rodriguez, A. L., Morrison, R. D., Venable, D. F., Manka, J. T., Bates, B. S., Blobaum, A. L., Byers, F. W., Daniels, J. S., Niswender, C. M., et al. (2013) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2013.09.001 · Cited by 33 · see citing works
Growth hormone signaling and hippocampal neurogenesis: Insights from genetic models
Ransome, M. I., & Turnley, A. M. (2008) · Hippocampus · doi:10.1002/hipo.20463 · Cited by 33 · see citing works
Nakaya, N., Sultana, A., Munasinghe, J., Cheng, A., Mattson, M. P., & Tomarev, S. I. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.09.019 · Cited by 32 · see citing works
Lee, K. M., Coelho, M. A., Class, M. A., & Szumlinski, K. K. (2018) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.10.031 · Cited by 32 · see citing works
de Brouwer, G., & Wolmarans, D. W. (2018) · Behavioural Processes · doi:10.1016/j.beproc.2018.04.011 · Cited by 32 · see citing works
Castro, G. P., Medeiros, D. D. C., Guarnieri, L. D. O., Mourão, F. A. G., Pinto, H. P. P., Pereira, G. S., & Moraes, M. F. D. (2015) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2015.08.039 · Cited by 32 · see citing works
Li, J., Liu, Q.-T., Chen, Y., Liu, J., Shi, J., Liu, Y., & Guo, J. (2016) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2016/6530364 · Cited by 32 · see citing works
Hybridizing behavioral models: A possible solution to some problems in neurophenotyping research?
Kalueff, A. V., LaPorte, J. L., Murphy, D. L., & Sufka, K. J. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.12.010 · Cited by 32 · see citing works
Sushma, G., Vaidya, B., Sharma, S., Devabattula, G., Bishnoi, M., Kondepudi, K. K., & Sharma, S. S. (2023) · Neuropharmacology · doi:10.1016/j.neuropharm.2023.109480 · Cited by 32 · see citing works
Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal
Turner, J. R., Wilkinson, D. S., Poole, R. L., Gould, T. J., Carlson, G. C., & Blendy, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.105 · Cited by 29 · see citing works
Goeldner, C., Spooren, W. P. J. M., Wichmann, J., & Prinssen, E. P. M. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2636-x · Cited by 30 · see citing works
Self-citationTorres–Lista, V., Pousa, S. L., & Giménez‐Llort, L. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.05.001 · Cited by 29 · see citing works
Neurobehavioral effects of neonatal opioid exposure in mice: Influence of the OPRM1 SNP
Robinson, S. A., Jones, A. D., Brynildsen, J. K., Ehrlich, M. E., & Blendy, J. A. (2019) · Addiction Biology · doi:10.1111/adb.12806 · Cited by 30 · see citing works
Brocco, M., Dekeyne, A., la Cour, C. M., Touzard, M., Girardon, S., Veiga, S., Nanteuil, G. D., A, T. R. D. J., Olivier, B., & Millan, M. J. (2008) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2008.06.002 · Cited by 30 · see citing works
Macrı̀, S., Ceci, C., Onori, M. P., Invernizzi, R. W., Bartolini, E., Altabella, L., Canese, R., Imperi, M., Orefici, G., Creti, R., et al. (2015) · Scientific Reports · doi:10.1038/srep13257 · Cited by 30 · see citing works
Exercise attenuates alveolar bone loss and anxiety‐like behaviour in rats with periodontitis
Andrade, E. F., Orlando, D. R., Gomes, J. A. S., Foureaux, R. D. C., Costa, R. C., Varaschin, M. S., Rogatto, G. P., de Moura, R. F., & Pereira, L. J. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12794 · Cited by 29 · see citing works
Kalinichev, M., Girard, F., Haddouk, H., Rouillier, M., Riguet, E., Royer-Urios, I., Mutel, V., Lütjens, R., & Poli, S. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.11.016 · Cited by 29 · see citing works
NOP Ligands for the Treatment of Anxiety and Mood Disorders
Gavioli, E. C., Holanda, V. A. D., & Ruzza, C. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_188 · Cited by 28 · see citing works
Kumar, V., Dey, A., & Chatterjee, S. (2018) · AYU (An International Quarterly Journal of Research in Ayurveda) · doi:10.4103/ayu.ayu_219_16 · Cited by 28 · see citing works
Rath, M., Guergues, J., Pinho, J. P. C., Zhang, P., Nguyen, T. G., MacFadyen, K. A., Peris, J., McLaughlin, J. P., Stevens, S. M., & Liu, B. (2020) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14420 · Cited by 29 · see citing works
Animal Behavior in Psychedelic Research
Odland, A. U., Kristensen, J. L., & Andreasen, J. T. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.122.000590 · Cited by 28 · see citing works
Millan, M. J., Gobert, A., Panayi, F., Rivet, J., Dekeyne, A., Brocco, M., Ortuno, J., & Cara, B. D. (2008) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145708008894 · Cited by 28 · see citing works
- Authors
- Nicolas, L. B., Kolb, Y., & Prinssen, E. P. M.
- Affiliations
- F. Hoffmann-La Roche AG (CH)
- Corresponding author
- Prinssen, Eric P.M.
- Venue
- European Journal of Pharmacology
- Publisher
- Elsevier BV
- Published
- 2006-10
- Volume
- 547
- Issue
- 1-3
- Pages
- 106-115
- ISSN
- 0014-2999 (ISSN-L)
- OpenAlex
- W2031480693
- Cited by
- 234
- References
- 41
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 18 · 2023: 11 · 2022: 7 · 2021: 18 · 2020: 12 · 2019: 12 · 2018: 12 · 2017: 13 · 2016: 13 · 2015: 18 · 2014: 11 · 2013: 13 · 2012: 9
- FWCI
- 4.18
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Pharmacology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Academy of Medical Sciences
- Akademie der Naturwissenschaften
- Schweizerische Akademie der Medizinischen Wissenschaften
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- marble burying test, locomotor activity, anxiety screening, anxiolytics, antidepressants, antipsychotic drugs, diazepam, fluoxetine, haloperidol, morphine, C57BL/6J mice, predictive validity, drug screening
- MeSH terms
- Animals, Antidepressive Agents, Behavior, Animal, Diazepam, Dose-Response Relationship, Drug, Drug Evaluation, Preclinical, Fluoxetine, Haloperidol, Imidazoles, Male, Mice, Inbred BALB C, Mice, Inbred CBA, Mice, Inbred C57BL, Morphine, Motor Activity, Obsessive-Compulsive Disorder, Pyridines, Species Specificity, Spiro Compounds, Antipsychotic Agents, Anti-Anxiety Agents, Reproducibility of Results, Mice
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