The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
Antagonistic Control of Social versus Repetitive Self-Grooming Behaviors by Separable Amygdala Neuronal Subsets
Open accessAbstract
Animals display a range of innate social behaviors that play essential roles in survival and reproduction. While the medial amygdala (MeA) has been implicated in prototypic social behaviors such as aggression, the circuit-level mechanisms controlling such behaviors are not well understood. Using cell-type-specific functional manipulations, we find that distinct neuronal populations in the MeA control different social and asocial behaviors. A GABAergic subpopulation promotes aggression and two other social behaviors, while neighboring glutamatergic neurons promote repetitive self-grooming, an asocial behavior. Moreover, this glutamatergic subpopulation inhibits social interactions independently of its effect to promote self-grooming, while the GABAergic subpopulation inhibits self-grooming, even in a nonsocial context. These data suggest that social versus repetitive asocial behaviors are controlled in an antagonistic manner by inhibitory versus excitatory amygdala subpopulations, respectively. These findings provide a framework for understanding circuit-level mechanisms underlying opponency between innate behaviors, with implications for their perturbation in psychiatric disorders.
Overview
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
Verification
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“While advanced circuit mapping tools have recently been effective at identifying specific nodes critical for sex-specific behaviors like mating, parenting, and aggression (Hong et al., 2014; Wu et al., 2009), many of these techniques rely on the use of transgenic mice, which, in contrast to rats, do not engage in tertiary social play.”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Hong et al., 2014
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“previous work has demonstrated that activation of GABAergic rather than glutamatergic neurons in the MeA is associated with onset of male aggression [82].”
In the citing paper
“The MeA has been subdivided into distinct functional regions along the anterior-posterior and dorsal-ventral axes, with the medial amygdala posterodorsal (MeApd) primarily involved in conspecific social behaviors such as mating and aggression (Choi et al., 2005; Hong et al., 2014).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Hong et al., 2014
In the citing paper
“The MeApd comprises GABAergic and glutamatergic neurons at an approximate ratio of 2:1, with GABAergic neurons representing the major population of projection neurons driving social responses (Choi et al., 2005; Hong et al., 2014; Keshavarzi et al., 2014).”
From Neuronal Representation of Social Information in the Medial Amygdala of Awake Behaving Mice (2017) · cites this paper as Hong et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,951
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907
Millisecond-timescale, genetically targeted optical control of neural activity
Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., & Deisseroth, K. A. (2005) · Nature Neuroscience · doi:10.1038/nn1525 · Cited by 5,015
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768
Neurodegenerative Disorders: Parkinson's Disease and Huntington's Disease
Hague, S., Klaffke, S., & Bandmann, O. (2006) · IMPERIAL COLLEGE PRESS eBooks · doi:10.1142/9781860948961_0007 · Cited by 2,767
Rowan, W., & Tinbergen, N. (1952) · Bird-Banding · doi:10.2307/4510368 · Cited by 2,706
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462
Swanson, L. W., & Petrovich, G. D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01265-x · Cited by 1,351
Leptin Action on GABAergic Neurons Prevents Obesity and Reduces Inhibitory Tone to POMC Neurons
Vong, L., Ye, C., Yang, Z., Choi, B. J., Chua, S. C., & Lowell, B. B. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.028 · Cited by 1,237
NEWMAN, S. W. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09271.x · Cited by 1,189
Baron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00011-7 · Cited by 1,130
Neural mechanisms of aggression
Nelson, R. J., & Trainor, B. C. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2174 · Cited by 1,046
Molecular and Cellular Approaches for Diversifying and Extending Optogenetics
Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., Goshen, I., Thompson, K. R., & Deisseroth, K. A. (2010) · Cell · doi:10.1016/j.cell.2010.02.037 · Cited by 1,040
Alexander, G. M., Rogan, S. C., Abbas, A. I., Armbruster, B. N., Pei, Y., Allen, J., Nonneman, R. J., Hartmann, J. F., Moy, S. S., Nicolelis, M. A. L., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.014 · Cited by 1,019
Pitkänen, A., Savander, V., & LeDoux, J. E. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01125-9 · Cited by 980
Aravanis, A. M., Wang, L., Zhang, F., Meltzer, L. A., Mogri, M., Schneider, M. B., & Deisseroth, K. A. (2007) · Journal of Neural Engineering · doi:10.1088/1741-2560/4/3/s02 · Cited by 960
Functional identification of an aggression locus in the mouse hypothalamus
Lin, D., Boyle, M. P., Dollar, P., Lee, H., Lein, E. S., Perona, P., & Anderson, D. J. (2011) · Nature · doi:10.1038/nature09736 · Cited by 914
Self-citationOrganization of projections from the medial nucleus of the amygdala: A PHAL study in the rat
Canteras, N. S., Simerly, R. B., & Swanson, L. W. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600203 · Cited by 897
Loss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2
Stowers, L., Holy, T. E., Meister, M., Dulac, C. G., & Koentges, G. (2002) · Science · doi:10.1126/science.1069259 · Cited by 880
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878
Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846
New Vistas on Amygdala Networks in Conditioned Fear
Paré, D., Quirk, G. J., & Ledoux, J. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00153.2004 · Cited by 841 · cited 1×
“, 1997; Swanson and Petrovich, 1998) and is anatomically distinct from amygdala nuclei involved in conditioned fear (Duvarci and Pare, 2014; Ehrlich et al., 2009; Paré et al., 2004).”
BackgroundAmygdala Microcircuits Controlling Learned Fear
Duvarci, S., & Pare, D. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.042 · Cited by 751
Topography of projections from amygdala to bed nuclei of the stria terminalis
Dong, H.-W., Petrovich, G. D., & Swanson, L. W. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00079-0 · Cited by 714
Yang, C. F., Chiang, M. C., Gray, D. C., Prabhakaran, M., Alvarado, M., Juntti, S. A., Unger, E. K., Wells, J. A., & Shah, N. M. (2013) · Cell · doi:10.1016/j.cell.2013.04.017 · Cited by 694
Molecular detection of pheromone signals in mammals: from genes to behaviour
Dulac, C. G., & Torello, A. T. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1140 · Cited by 662
The Intense World Theory – A Unifying Theory of the Neurobiology of Autism
Markram, H., & Markram, H. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00224 · Cited by 571
Canteras, N. S., Simerly, R. B., & Swanson, L. W. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480103 · Cited by 565
Identification of protein pheromones that promote aggressive behaviour
Chamero, P., Marton, T. F., Logan, D. W., Flanagan, K. A., Cruz, J. R., Saghatelian, A., Cravatt, B. F., & Stowers, L. (2007) · Nature · doi:10.1038/nature05997 · Cited by 529
Fatemi, S. H., Halt, A. R., Stary, J. M., Kanodia, R., Schulz, S. C., & Realmuto, G. R. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01430-0 · Cited by 500
Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus
Lee, H., Kim, D.-W., Remedios, R., Anthony, T. E., Chang, A., Madisen, L., Zeng, H., & Anderson, D. J. (2014) · Nature · doi:10.1038/nature13169 · Cited by 479
Self-citationChoi, G. B., Dong, H.-W., Murphy, A. J., Valenzuela, D. M., Yancopoulos, G. D., Swanson, L. W., & Anderson, D. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.011 · Cited by 462
Self-citationNeuroligin-1 Deletion Results in Impaired Spatial Memory and Increased Repetitive Behavior
Blundell, J., Blaiss, C. A., Etherton, M. R., Espinosa, F., Tabuchi, K., Walz, C., Bolliger, M. F., Südhof, T. C., & Powell, C. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4517-09.2010 · Cited by 450
Etherton, M. R., Blaiss, C. A., Powell, C. M., & Südhof, T. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910297106 · Cited by 447
Olfactory Inputs to Hypothalamic Neurons Controlling Reproduction and Fertility
Yoon, H., Enquist, L. W., & Dulac, C. G. (2005) · Cell · doi:10.1016/j.cell.2005.08.039 · Cited by 435
Neuropharmacology of brain-stimulation-evoked aggression
Siegel, A., Roeling, T. A. P., Gregg, T. R., & Kruk, M. R. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00040-2 · Cited by 381
Influence of amygdalectomy on social behavior in monkeys.
Rosvold, H. E., Mirsky, A. F., & Pribram, K. H. (1954) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0058870 · Cited by 331
Linkage and association of the glutamate receptor 6 gene with autism
Jamain, S., Betancur, C., Quach, H., Philippe, A., Fellous, M., Giros, B., Gillberg, C., Leboyer, M., & Bourgeron, T. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4000979 · Cited by 318
Kollack‐Walker, S., & Newman, S. W. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00563-k · Cited by 315
Medial Nucleus of the Amygdala Mediates Chemosensory Control of Male Hamster Sexual Behavior
Lehman, M. N., Winans, S. S., & Powers, J. B. (1980) · Science · doi:10.1126/science.7423209 · Cited by 282
Modular Genetic Control of Sexually Dimorphic Behaviors
Xu, X., Coats, J., Yang, C. F., Wang, A., Ahmed, O. M., Alvarado, M., Izumi, T., & Shah, N. M. (2012) · Cell · doi:10.1016/j.cell.2011.12.018 · Cited by 273
Deficits in sexual and aggressive behaviors in Cnga2 mutant mice
Mandiyan, V. S., Coats, J., & Shah, N. M. (2005) · Nature Neuroscience · doi:10.1038/nn1589 · Cited by 270
Couture, S. M., Penn, D. L., Losh, M. C., Adolphs, R., Hurley, R. S. E., & Piven, J. (2009) · Psychological Medicine · doi:10.1017/s003329170999078x · Cited by 246
Sex-specific processing of social cues in the medial amygdala
Bergan, J. F., Ben-Shaul, Y., & Dulac, C. (2014) · eLife · doi:10.7554/elife.02743 · Cited by 237
Behavioral abnormality and pharmacologic response in social isolation-reared mice
Koike, H., Ibi, D., Mizoguchi, H., Nagai, T., Nitta, A., Takuma, K., Nabeshima, T., Yoneda, Y., & Yamada, K. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.03.028 · Cited by 227
Toward a Neural Basis for Social Behavior
Stanley, D. A., & Adolphs, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.038 · Cited by 213
Orienting to social stimuli differentiates social cognitive impairment in autism and schizophrenia
Sasson, N., Tsuchiya, N., Hurley, R., Couture, S. M., Penn, D. L., Adolphs, R., & Piven, J. (2007) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2007.03.009 · Cited by 201
Ethology and pharmacology of hypothalamic aggression in the rat
Kruk, M. R. (1991) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80144-7 · Cited by 166
Kondo, Y. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90074-c · Cited by 163
Problems in the study of rodent aggression
Blanchard, R. J., Wall, P. M., & Blanchard, D. C. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00127-2 · Cited by 160
Veening, J. G., Coolen, L. M., A, T. R. D. J., Joosten, H. W. J., de Boer, S. F., Koolhaas, J. M., & Olivier, B. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.09.041 · Cited by 156
Williams, J. H. G. (2008) · Autism Research · doi:10.1002/aur.15 · Cited by 148
Early social deprivation induces disturbed social communication and violent aggression in adulthood.
Tóth, M., Halász, J., Mikics, É., Barsy, B., & Haller, J. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.4.849 · Cited by 135
The hypothalamus: cross-roads of endocrine and behavioural regulation in grooming and aggression
Kruk, M. R., Westphal, K. G. C., van Erp, A. M. M., van Asperen, J., Cave, B. J., Slater, E., de Koning, J., & Haller, J. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00018-9 · Cited by 123
Medial amygdala lesions in male rats reduce aggressive behavior: interference with experience
Vochteloo, J. D., & Koolhaas, J. M. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90137-5 · Cited by 109
Kollack, S. S., & Newman, S. W. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90270-h · Cited by 102
Mating-induced increases in FOS protein in preoptic area and medial amygdala of cycling female rats
Erskine, M. S. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90289-n · Cited by 98
Zufall, F., & Leinders‐Zufall, T. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.07.012 · Cited by 98
Brain mechanisms of aggressive behavior: an updated review.
Adams, D. B. (2006) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.09.004 · Cited by 97
Kondo, Y., & Arai, Y. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00205-j · Cited by 92
Cortical-Like Functional Organization of the Pheromone-Processing Circuits in the Medial Amygdala
Bian, X., Yanagawa, Y., Chen, W. R., & Luo, M. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00902.2007 · Cited by 92
Taming in wild rats following medial amygdaloid lesions
Kemble, E. D., Blanchard, D. C., Blanchard, R. J., & Takushi, R. Y. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90084-2 · Cited by 70
Wang, Y., He, Z., Zhao, C., & Li, L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.02.002 · Cited by 59
A failure of amygdaloid lesions to alter agonistic behavior in the laboratory rat
Busch, D. E., & Barfield, R. J. (1974) · Physiology & Behavior · doi:10.1016/0031-9384(74)90027-4 · Cited by 58
Comparing social attention in autism and amygdala lesions: Effects of stimulus and task condition
Birmingham, E., Cerf, M., & Adolphs, R. (2011) · Social Neuroscience · doi:10.1080/17470919.2011.561547 · Cited by 56
Takahashi, L. K., & Gladstone, C. D. (1988) · Behavioral Neuroscience · doi:10.1037//0735-7044.102.2.268 · Cited by 42
Takahashi, L. K., & Gladstone, C. D. (1988) · Behavioral Neuroscience · doi:10.1037/0735-7044.102.2.268 · Cited by 35
Dhungel, S., Masaoka, M., Rai, D., Kondo, Y., & Sakuma, Y. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.09.051 · Cited by 32
Niimi, K., Horie, S., Yokosuka, M., Kawakami-Mori, F., Tanaka, K., Fukayama, H., & Sahara, Y. (2012) · Brain Research · doi:10.1016/j.brainres.2012.08.050 · Cited by 14
Cited by
Sorted by citations
Ventromedial hypothalamic neurons control a defensive emotion state
Kunwar, P. S., Zelikowsky, M., Remedios, R., Cai, H., Balban, M. Y., Meister, M., & Anderson, D. J. (2015) · eLife · doi:10.7554/elife.06633 · Cited by 1,130
Self-citationNeurobiology of rodent self-grooming and its value for translational neuroscience
Kalueff, A. V., Stewart, A. M., Song, C., Berridge, K. C., Graybiel, A. M., & Fentress, J. C. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.8 · Cited by 852
Neural circuit mechanisms of social behavior
Chen, P., & Hong, W. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.026 · Cited by 527
Self-citationFunctional circuit architecture underlying parental behaviour
Kohl, J., Babayan, B. M., Rubinstein, N. D., Autry, A. E., Marin-Rodriguez, B., Kapoor, V., Miyamichi, K., Zweifel, L. S., Luo, L., Uchida, N., et al. (2018) · Nature · doi:10.1038/s41586-018-0027-0 · Cited by 470
Brain circuit dysfunction in post-traumatic stress disorder: from mouse to man
Fenster, R. J., Lebois, L. A. M., Ressler, K. J., & Suh, J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0039-7 · Cited by 456
Metadata
- Authors
- Hong, W., Kim, D.-W., & Anderson, D. J.
- Affiliations
- California Institute of Technology (US)
- Corresponding author
- Anderson, David J.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2014-09
- Volume
- 158
- Issue
- 6
- Pages
- 1348-1361
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4167378
- OpenAlex
- W2065254519
- Cited by
- 405
- References
- 68
- Citations by year
- 2026: 17 · 2025: 39 · 2024: 32 · 2023: 38 · 2022: 39 · 2021: 45 · 2020: 51 · 2019: 29 · 2018: 30 · 2017: 31 · 2016: 25 · 2015: 25 · 2014: 3
- FWCI
- 15.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Simons Foundation
- California Institute of Technology
- National Institutes of Health
- National Institute of Mental Health (MH085082, MH070053, R01MH085082, R01MH070053)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- medial amygdala, social behavior, aggression, GABAergic neurons, glutamatergic neurons, neuronal subpopulations, asocial behavior
- MeSH terms
- Aggression, Amygdala, Animals, Female, gamma-Aminobutyric Acid, Grooming, Male, Mice, Inbred BALB C, Mice, Inbred C57BL, Neurons, Social Behavior, Mice, In Vitro Techniques
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
