Expression and pharmacological modulation of visceral pain-induced conditioned place aversion in mice
Open accessAbstract
Pain encompasses both a sensory as well as an affective dimension and these are differentially processed in the brain and periphery. It is therefore important to develop animal models to reflect the non-reflexive assays in pain. In this study, we compared effects of the mu opioid receptor agonist morphine, the nonsteroidal anti-inflammatory drug ketoprofen and the kappa receptor opioid agonist U50,488H and antagonist JDTic on acetic acid-induced stretching and acetic acid-induced aversion in the condition place aversion (CPA) test in male ICR mice. Intraperitoneal administration of acetic acid (0.32-1%) was equipotent in stimulating stretching and CPA. Ketoprofen, morphine and U50,488H all inhibited the acid-induced stretching. Ketoprofen and morphine also blocked the acid-induced CPA but U50,488H failed to do so. The reversal ability of ketoprofen and morphine on acid-induced CPA is unique to pain-stimulated place aversion since these drugs failed to reduce non-noxious LiCl-induced CPA. Overall, this study characterized and validated a preclinical mouse model of pain-related aversive behavior that can be used to assess genetic and biological mechanisms of pain as well as improving the predictive validity of preclinical studies on candidate analgesics.
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
Cites
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?
Systemic JDtic fails to block conditioned place aversion produced by visceral and acid-induced pain in mice.
“However, systemic doses of the k-opioid receptor antagonist (3R)-7-hydroxy-N-{(2S)-1-[(3R,4R)-4-(3-hydroxyphenyl)-3,4-dimethylpiperidin-1yl]-3-methylbutan-2-yl}-1,2,3,4-tetrahydroisoquinoline-3-carboxamide (JDtic) failed to block conditioned place aversion that was produced by visceral and acid-induced pain in mice (Bagdas et al., 2016).”
From Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development (2021) · cites this paper as Bagdas et al., 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Animal models of pain: progress and challenges
Mogil, J. S. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2606 · Cited by 1,126 · see citing works
Johansen, J. P., Fields, H. L., & Manning, B. H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141218998 · Cited by 677 · see citing works
Chronic pain patients are impaired on an emotional decision-making task
Apkarian, V. A., Sosa, Y., Krauss, B. R., Thomas, S. P., Fredrickson, B. E., Levy, R. E., Harden, N. R., & Chialvo, D. R. (2004) · Pain · doi:10.1016/j.pain.2003.12.015 · Cited by 536 · see citing works
Apoptotic cell: linkage of inflammation and wound healing
Wu, Y.-S., & Chen, S.-N. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00001 · Cited by 500 · see citing works
The mouse ascending: perspectives for human-disease models
Rosenthal, N., & Brown, S. (2007) · Nature Cell Biology · doi:10.1038/ncb437 · Cited by 442 · see citing works
Manual of Pharmacologic Calculations
Tallarida, R. J., & Murray, R. B. (1987) · Springer eBooks · doi:10.1007/978-1-4612-4974-0 · Cited by 429 · see citing works
Cognitive Impairment in Pain through Amygdala-Driven Prefrontal Cortical Deactivation
Ji, G., Sun, H., Fu, Y., Li, Z., Pais-Vieira, M., Galhardo, V., & Neugebauer, V. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0225-10.2010 · Cited by 387 · see citing works
Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal
Johansen, J. P., & Fields, H. L. (2004) · Nature Neuroscience · doi:10.1038/nn1207 · Cited by 365 · see citing works
Neugebauer, V., Galhardo, V., Maione, S., & Mackey, S. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.12.014 · Cited by 353 · see citing works
Preclinical Assessment of Candidate Analgesic Drugs: Recent Advances and Future Challenges
Negus, S. S., Vanderah, T. W., Brandt, M. R., Bilsky, E. J., Becerra, L. R., & Borsook, D. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.106377 · Cited by 255 · see citing works
Self-citationCobos, E. J., Ghasemlou, N., Araldi, D., Segal, D., Duong, K., & Woolf, C. J. (2012) · Pain · doi:10.1016/j.pain.2012.01.016 · Cited by 240 · see citing works
LaBuda, C. J., & Fuchs, P. N. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7395 · Cited by 237 · see citing works
Clinical and pre-clinical pain assessment: Are we measuring the same thing?
Vierck, C. J., Hansson, P. T., & Yezierski, R. P. (2008) · Pain · doi:10.1016/j.pain.2007.12.008 · Cited by 205 · see citing works
Remote Optogenetic Activation and Sensitization of Pain Pathways in Freely Moving Mice
Daou, I., Tuttle, A. H., Longo, G., Wieskopf, J. S., Bonin, R. P., Ase, A. R., Wood, J. N., De Koninck, Y., Ribeiro-da-Silva, A., Mogil, J. S., et al. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2424-13.2013 · Cited by 175 · see citing works
Tanimoto, S., Nakagawa, T., Yamauchi, Y., Minami, M., & Satoh, M. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02952.x · Cited by 159 · see citing works
Broadbear, J. H., Negus, S. S., Butelman, E. R., de Costa, B. R., & Woods, J. H. (1994) · Psychopharmacology · doi:10.1007/bf02245071 · Cited by 139 · see citing works
Self-citationMartin, T. J., Buechler, N. L., Kahn, W., Crews, J. C., & Eisenach, J. C. (2004) · Anesthesiology · doi:10.1097/00000542-200407000-00030 · Cited by 131 · see citing works
Stevenson, G. W., Bilsky, E. J., & Negus, S. S. (2006) · Journal of Pain · doi:10.1016/j.jpain.2006.01.447 · Cited by 105 · see citing works
Self-citationDoes the kappa opioid receptor system contribute to pain aversion?
Cahill, C. M., Taylor, A. M. W., Cook, C., Ong, E., Morón, J. A., & Evans, C. J. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00253 · Cited by 105 · see citing works
Analgesic Efficacy of Enadoline Versus Placebo or Morphine in Postsurgical Pain
Pande, A. C., Pyke, R. E., Greiner, M., Wideman, G. L., Benjamin, R., & Pierce, M. (1996) · Clinical Neuropharmacology · doi:10.1097/00002826-199619050-00009 · Cited by 91 · see citing works
Effects of ketoprofen, morphine, and kappa opioids on pain-related depression of nesting in mice
Negus, S. S., Neddenriep, B., Altarifi, A., Carroll, F. I., Leitl, M. D., & Miller, L. L. (2015) · Pain · doi:10.1097/j.pain.0000000000000171 · Cited by 88 · see citing works
Self-citationLeitl, M. D., Onvani, S., Bowers, M. S., Cheng, K., Rice, K. C., Carlezon, W. A., Banks, M. L., & Negus, S. S. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.236 · Cited by 87 · see citing works
Self-citationPapke, R. L., Bağdaş, D., Kulkarni, A., Gould, T., AlSharari, S. D., Thakur, G. A., & Damaj, M. I. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.002 · Cited by 87 · see citing works
Self-citationHummel, M., Lu, P., Cummons, T. A., & Whiteside, G. T. (2008) · Pain · doi:10.1016/j.pain.2008.09.020 · Cited by 83 · see citing works
Thomas, J. B., Atkinson, R. N., Vinson, N. A., et al. (2003) · Journal of Medicinal Chemistry · doi:10.1021/jm030094y · Cited by 76 · see citing works
van der Kam, E. L., Vry, J. D., Schiene, K., & Tzschentke, T. (2007) · Pain · doi:10.1016/j.pain.2007.07.027 · Cited by 74 · see citing works
Deyama, S., Katayama, T., Ohno, A., Nakagawa, T., Kaneko, S., Yamaguchi, T., Yoshioka, M., & Minami, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1480-08.2008 · Cited by 71 · see citing works
Effects of kappa opioids in an assay of pain-depressed intracranial self-stimulation in rats
Negus, S. S., Morrissey, E. M., Rosenberg, M., Cheng, K., & Rice, K. C. (2010) · Psychopharmacology · doi:10.1007/s00213-009-1770-6 · Cited by 66 · see citing works
Self-citationHoran, P. J., de Costa, B. R., Rice, K. C., et al. (1991) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24685-7 · Cited by 65 · see citing works
Stevenson, G. W., Cormier, J., Mercer, H., Adams, C., Dunbar, C., Negus, S. S., & Bilsky, E. J. (2009) · Life Sciences · doi:10.1016/j.lfs.2009.06.006 · Cited by 63 · see citing works
Self-citationLeitl, M. D., Potter, D. N., Cheng, K., Rice, K. C., Carlezon, W. A., & Negus, S. S. (2014) · Molecular Pain · doi:10.1186/1744-8069-10-62 · Cited by 62 · see citing works
Self-citationAnalgesic Efficacy of the κ-Receptor Agonist, Enadoline, in Dental Surgery Pain
Pande, A. C., Pyke, R. E., Greiner, M., Cooper, S. A., Benjamin, R., & Pierce, M. (1996) · Clinical Neuropharmacology · doi:10.1097/00002826-199619010-00009 · Cited by 61 · see citing works
Negus, S. S., O’Connell, R., Morrissey, E. M., Cheng, K., & Rice, K. C. (2011) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.111.186783 · Cited by 60 · see citing works
Self-citationDeyama, S., Nakagawa, T., Kaneko, S., Uehara, T., & Minami, M. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.10.021 · Cited by 59 · see citing works
Carmo, G. P. D., Folk, J. E., Rice, K. C., Chartoff, E. H., Carlezon, W. A., & Negus, S. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.12.021 · Cited by 55 · see citing works
Self-citationAn industry perspective on the role and utility of animal models of pain in drug discovery
Whiteside, G. T., Pomonis, J. D., & Kennedy, J. D. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.08.033 · Cited by 52 · see citing works
The painlike effect of gallamine and naloxone differs from sickness induced by lithium chloride.
Lett, B. T. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.1.145 · Cited by 46 · see citing works
Frisch, C., Hasenöhrl, R. U., Mattern, C., et al. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00073-6 · Cited by 43 · see citing works
The application of conditioning paradigms in the measurement of pain
Li, J. (2013) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2013.03.002 · Cited by 40 · see citing works
The painlike effect of gallamine and naloxone differs from sickness induced by lithium chloride.
Lett, B. T. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.1.145 · Cited by 40 · see citing works
Zhang, R.-X., Zhang, M., Li, A., Pan, L., Berman, B., Ren, K., & Lao, L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.030 · Cited by 29 · see citing works
Animal models of pain for drug discovery
Joshi, S. K., & Honoré, P. (2006) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.1.4.323 · Cited by 23 · see citing works
Deyama, S., Takishita, A., Tanimoto, S., et al. (2010) · Journal of Pharmacological Sciences · doi:10.1254/jphs.10139sc · Cited by 14 · see citing works
Rinaman, L., Saboury, M., & Litvina, E. Y. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.017 · Cited by 12 · see citing works
Roles of corticosterone in formalin-induced conditioned place aversion in rats
Wang, H., Wang, Y., Huang, A. C. W., Chai, S.-C., Wu, Y.-S., & Wang, C. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.08.053 · Cited by 10 · see citing works
Browne, L. E., & Woolf, C. J. (2014) · Nature Biotechnology · doi:10.1038/nbt.2844 · Cited by 3 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Rivière PJM Junien JL 2000 Opioid receptors, targets for new gastrointestinal drug development Drug Development Molecular Targets for GI Diseases Totowa, NJ Humana Press 203 238 Gaginella TS Guglietta A
Cited by
Sorted by citations
Drug Addiction: Hyperkatifeia/Negative Reinforcement as a Framework for Medications Development
Koob, G. F. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000083 · Cited by 337 · see citing works
- Authors
- Bagdas, D., Muldoon, P. P., AlSharari, S., Carroll, F. I., Negus, S. S., & Damaj, M. I.
- Affiliations
- Virginia Commonwealth University (US)
- RTI International (US)
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 102
- Pages
- 236-243
- ISSN
- 0028-3908 (ISSN-L)
- PMC
- PMC5574195
- OpenAlex
- W2173038123
- Cited by
- 39
- References
- 46
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 1 · 2023: 5 · 2022: 5 · 2021: 7 · 2020: 7 · 2019: 4 · 2018: 4 · 2017: 1
- FWCI
- 1.23
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Neuropharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Bursa Uludag University - AVESIS (submittedVersion)
- Funders
- NIH (R01DA-019377, R01NS070715, R01DA030404)
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- visceral pain, conditioned place aversion, acetic acid-induced pain, morphine, ketoprofen, U50,488H, JDTic, mu-opioid receptor, kappa opioid receptor, nonsteroidal anti-inflammatory drugs
- MeSH terms
- Analgesics, Opioid, Animals, Anti-Inflammatory Agents, Non-Steroidal, Avoidance Learning, Behavior, Animal, Ketoprofen, Male, Mice, Inbred ICR, Morphine, Piperidines, Receptors, Opioid, mu, Receptors, Opioid, kappa, 3,4-Dichloro-N-methyl-N-(2-(1-pyrrolidinyl)-cyclohexyl)-benzeneacetamide, (trans)-Isomer, Tetrahydroisoquinolines, Mice, Visceral Pain
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