Novel unconditioned prosocial behavior in prairie voles (Microtus ochrogaster) as a model for empathy
Open accessAbstract
OBJECTIVE: In this study, empathy is quantified using a novel social test. Empathy and prosocial behavior are linked to the expression of oxytocin in humans and rodent models. Specifically, prosocial behavior in prairie voles (Microtus ochrogaster) has been linked to the expression of oxytocin in the paraventricular nucleus of the hypothalamus. The animal's behavior was considered empathic if it spends significantly more time attempting to remove a loos fitting restraint (tether) from the stimulus animal than time in contact with a, simultaneously presented, non-social object similar to the tether. The behavioral data was cross-referenced with the number of neurons expressing oxytocin and arginine vasopressin, as well as the density of dopaminergic neurons (identified by the expression of tyrosine hydroxylase), in the paraventricular nucleus of the hypothalamus. These proteins influence empathic behavior in humans, non-human primates, rats, mice, and prairie voles. RESULTS: The consistency between neuroanatomical mechanisms linked to empathy, and the durations of time spent engaging in empathic contact, support the prediction that the empathic contact in this test is a distinct prosocial behavior, lacking prior behavioral training or the naturally occurring ethological relevance of other prosocial behaviors, and is a measure of empathy.
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?
Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation.
“Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation (Burkett et al., 2016; Stetzik et al., 2018; Wardwell et al., 2020).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Stetzik et al., 2018
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
Vӧllm, B., Taylor, A. N. W., Richardson, P., Corcoran, R., Stirling, J., McKie, S., Deakin, J. F. W., & Elliott, R. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.07.022 · Cited by 1,004 · see citing works
Empathy and pro-social behavior in rats
Bartal, I. B.-A., Decety, J., & Mason, P. (2011) · Science · doi:10.1126/science.1210789 · Cited by 934 · see citing works
Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans
Hurlemann, R., Patin, A., Onur, O. A., Cohen, M. X., Baumgartner, T., Metzler, S., Dziobek, I., Gallinat, J., Wagner, M., Maier, W., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5538-09.2010 · Cited by 771 · see citing works
Oxytocin-dependent consolation behavior in rodents
Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016) · Science · doi:10.1126/science.aac4785 · Cited by 692 · see citing works
Noninvasive optical inhibition with a red-shifted microbial rhodopsin
Miri, M. L., Busskamp, V., Young, A., Ogawa, M., Ramanlal, S. B., Forest, C. R., Chow, B. Y., Han, X., Lin, Y., Roska, B., et al. (2014) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 554 · see citing works
Oxytocin Attenuates Affective Evaluations of Conditioned Faces and Amygdala Activity
Petrovic, P., Kalisch, R., Singer, T., & Dolan, R. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4572-07.2008 · Cited by 424 · see citing works
The neurobiology of pair bonding: Insights from a socially monogamous rodent
Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.006 · Cited by 389 · see citing works
Oxytocin enhances social recognition by modulating cortical control of early olfactory processing
Oettl, L.-L., Ravi, N., Schneider, M., Scheller, M. F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R. C., Chao, M. V., Young, W. S., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.033 · Cited by 359 · see citing works
Auditory sensitivity of the albino rat.
Kelly, J. B., & Masterton, B. (1977) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077356 · Cited by 353 · see citing works
Bethlehem, R. A. I., van Honk, J., Auyeung, B., & Baron-Cohen, S. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.10.011 · Cited by 285 · see citing works
Carter, C. S., Getz, L. L., Gavish, L., Dermott, J. L. M., & Arnold, P. (1980) · Biology of Reproduction · doi:10.1095/biolreprod23.5.1038 · Cited by 242 · see citing works
Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization
Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015077 · Cited by 216 · see citing works
Mating in the monogamous male: Behavioral consequences
Insel, T. R., Preston, S., & Winslow, J. T. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00362-9 · Cited by 215 · see citing works
Arginine Vasopressin and Oxytocin Modulate Human Social Behavior
Ebstein, R. P., Israel, S., Lerer, E., Uzefovsky, F., Shalev, I., Gritsenko, I., Riebold, M., Salomon, S., & Yirmiya, N. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04541.x · Cited by 194 · see citing works
Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.004 · Cited by 192 · see citing works
The roots of empathy: Through the lens of rodent models
Meyza, K. Z., Bartal, I. B.-A., Monfils, M., Panksepp, J. B., & Knapska, E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.10.028 · Cited by 167 · see citing works
Oxytocin enhances observational fear in mice
Pisansky, M. T., Hanson, L. R., Gottesman, I. I., & Gewirtz, J. C. (2017) · Nature Communications · doi:10.1038/s41467-017-02279-5 · Cited by 167 · see citing works
Yamamoto, Y., Cushing, B. S., Kramer, K. M., Epperson, P. D., Hoffman, G. E., & Carter, C. S. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.02.028 · Cited by 155 · see citing works
Peripheral Pulses of Oxytocin Increase Partner Preferences in Female, but Not Male, Prairie Voles
Cushing, B. S., & Carter, C. S. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1558 · Cited by 136 · see citing works
Uzefovsky, F., Shalev, I., Israel, S., Edelman, S., Raz, Y., Mankuta, D., Knafo-Noam, A., & Ebstein, R. P. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.11.007 · Cited by 131 · see citing works
Liu, Y., Aragona, B. J., Young, K. A., Dietz, D. M., Kabbaj, M., Mazei-Robison, M., Nestler, E. J., & Wang, Z. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911998107 · Cited by 101 · see citing works
The effects of peptides on partner preference formation are predicted by habitat in prairie voles
Cushing, B. S., Martin, J. O., Young, L. J., & Carter, C. S. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2000.1633 · Cited by 99 · see citing works
Self-citationOxytocin increases empathy to pain when adopting the other-but not the self-perspective
Abu-Akel, A., Palgi, S., Klein, E., Decety, J., & Shamay-Tsoory, S. (2015) · Social Neuroscience · doi:10.1080/17470919.2014.948637 · Cited by 83 · see citing works
Dominance status predicts social fear transmission in laboratory rats
Jones, C. E., & Monfils, M.-H. (2016) · Animal Cognition · doi:10.1007/s10071-016-1013-2 · Cited by 81 · see citing works
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79 · see citing works
Perkeybile, A. M., Delaney-Busch, N., Hartman, S., Grimm, K. J., & Bales, K. L. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00191 · Cited by 76 · see citing works
Oxytocin and vasopressin: Social neuropeptides with complex neuromodulatory functions
Benarroch, E. E. (2013) · Neurology · doi:10.1212/wnl.0b013e31828cfb15 · Cited by 74 · see citing works
Kim, B. S., Lee, J., Bang, M., Seo, B. A., Khalid, A., Jung, M. W., & Jeon, D. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3581-7 · Cited by 65 · see citing works
Effects of hormonal, sexual, and social history on mating and pair bonding in prairie voles
Carter, C. S., Witt, D. M., Thompson, E. G., & Carlstead, K. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90049-2 · Cited by 64 · see citing works
Lü, Y.-F., Ren, B., Ling, B.-F., Zhang, J., Chen, X., & Li, Z. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.10.063 · Cited by 62 · see citing works
On the neglected role of stereotypes in empathy toward other-race pain
Meconi, F., Vaes, J., & Sessa, P. (2014) · Social Neuroscience · doi:10.1080/17470919.2014.954731 · Cited by 46 · see citing works
Lü, Y.-F., Yang, Y. L., Li, C.-L., Wang, Y., Li, Z., & Chen, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00066 · Cited by 44 · see citing works
Noninvasive optical inhibition with a red-shifted microbial rhodopsin
Chuong, A. S., Miri, M. L., Busskamp, V., Matthews, G. A. C., Acker, L. C., Sørensen, A. T., Young, A., Klapoetke, N. C., Henninger, M. A., Kodandaramaiah, S. B., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3752 · Cited by 33 · see citing works
Dharmadhikari, A., LEE, Y. S., Roberts, R. L., & Carter, C. S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51982.x · Cited by 23 · see citing works
Cavanaugh, B. L., & Lonstein, J. S. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.01958.x · Cited by 23 · see citing works
Fontenot, J., Loetz, E. C., Ishiki, M., & Bland, S. T. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.038 · Cited by 19 · see citing works
Stetzik, L. A., Ganshevsky, D., Lende, M. N., Roache, L. E., Musatov, S. A., & Cushing, B. S. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.035 · Cited by 18 · see citing works
The organizational effects of oxytocin and vasopressin: Behavioral implications
Cushing, B. S. (2013) · Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior · doi:10.1017/cbo9781139017855.006 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Gillera, S. E. A., Marinello, W. P., Horman, B. M., Phillips, A. L., Ruis, M. T., Stapleton, H. M., Reif, D. M., & Patisaul, H. B. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106840 · Cited by 48 · see citing works
Helping behavior in prairie voles: a model of empathy and the importance of oxytocin
Kitano, K., Yamagishi, A., Horie, K., Nishimori, K., & Sato, N. (2022) · iScience · doi:10.1016/j.isci.2022.103991 · Cited by 31 · see citing works
Are There Multiple Motivators for Helping Behavior in Rats?
Silva, P. R. R., Silva, R. H., Lima, R. H., Meurer, Y. D. S. R., Ceppi, B., & Yamamoto, M. E. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.01795 · Cited by 25 · see citing works
Kentrop, J., Kalamari, A., Danesi, C. H., Kentrop, J. J., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Joëls, M., & van der Veen, R. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100827 · Cited by 25 · see citing works
Current rodent models for the study of empathic processes
Cox, S. S., & Reichel, C. M. (2020) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000590 · Cited by 15 · see citing works
Gillera, S. E. A., Marinello, W. P., Nelson, M. A., Horman, B. M., & Patisaul, H. B. (2022) · Toxics · doi:10.3390/toxics10050268 · Cited by 11 · see citing works
Identification of hippocampal area CA2 in hamster and vole brain
Siegler, P. N., Shaughnessy, E. K., Horman, B. M., Vierling, T. T., King, D. H., Patisaul, H. B., Huhman, K. L., Alexander, G. M., & Dudek, S. M. (2024) · The Journal of Comparative Neurology · doi:10.1002/cne.25603 · Cited by 6 · see citing works
Evidence for the involvement of a fronto-striatal pathway in the processing of social reward
Lin, K., & Coutellier, L. D. (2025) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2025.102834 · Cited by 6 · see citing works
Walker, S. L., & Glasper, E. R. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101162 · Cited by 3 · see citing works
Automatic reconstruction of metabolic pathways from identified biosynthetic gene clustersPreprint
Sulheim, S., Fossheim, F. A., Wentzel, A., & Almaas, E. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.24.395400 · Cited by 1 · see citing works
- Authors
- Stetzik, L. A., Sullivan, A. W., Patisaul, H. B., & Cushing, B. S.
- Affiliations
- University of Akron (US)
- North Carolina State University (US)
- The University of Texas at El Paso (US)
- Corresponding author
- Stetzik, Lucas A.
- Venue
- BMC Research Notes
- Published
- 2018-12
- Volume
- 11
- Issue
- 1
- Pages
- 852-852
- ISSN
- 1756-0500 (ISSN-L)
- PMC
- PMC6278148
- OpenAlex
- W2903288152
- Cited by
- 10
- References
- 37
- Citations by year
- 2025: 1 · 2024: 2 · 2022: 1 · 2021: 1 · 2020: 4 · 2019: 1
- FWCI
- 2.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- BMC Research Notes (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Florida Digital Collections (University of Florida) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Environmental Health Sciences (ES021233)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Keywords
- empathy, prosocial behavior, Microtus ochrogaster, oxytocin, vasopressin, paraventricular nucleus, dopaminergic neurons, tyrosine hydroxylase
- MeSH terms
- Animals, Arginine Vasopressin, Behavior, Animal, Cooperative Behavior, Arvicolinae, Empathy, Female, Humans, Hypothalamus, Male, Oxytocin, Paraventricular Hypothalamic Nucleus, Tyrosine 3-Monooxygenase, Gene Expression, Models, Animal, Dopaminergic Neurons
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