Skip to main content
Log in

Transcriptomic Analysis Reveals Sex-Dependent Expression Patterns in the Basolateral Amygdala of Dominant and Subordinate Animals After Acute Social Conflict

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

The basolateral amygdala (BLA) is a critical nucleus mediating behavioral responses after exposure to acute social conflict. Male and female Syrian hamsters both readily establish a stable dominant-subordinate relationship among same-sex conspecifics, and the goal of the current study was to determine potential underlying genetic mechanisms in the BLA facilitating the establishment of social hierarchy. We sequenced the BLA transcriptomes of dominant, subordinate, and socially neutral males and females, and using de novo assembly techniques and gene network analyses, we compared these transcriptomes across social status within each sex. Our results revealed 499 transcripts that were differentially expressed in the BLA across both males and females and 138 distinct gene networks. Surprisingly, we found that there was virtually no overlap in the transcript changes or in gene network patterns in males and females of the same social status. These results suggest that, although males and females reliably engage in similar social behaviors to establish social dominance, the molecular mechanisms in the BLA by which these statuses are obtained and maintained are distinct.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Bjorkqvist K (2001) Social defeat as a stressor in humans. Physiol Behav 73(3):435–442

    Article  CAS  Google Scholar 

  2. Agid O, Kohn Y, Lerer B (2000) Environmental stress and psychiatric illness. Biomed Pharmacother 54(3):135–141. https://doi.org/10.1016/s0753-3322(00)89046-0

    Article  CAS  PubMed  Google Scholar 

  3. Ehlers A, Maercker A, Boos A (2000) Posttraumatic stress disorder following political imprisonment: The role of mental defeat, alienation, and perceived permanent change. J Abnorm Psychol 109(1):45–55

    Article  CAS  Google Scholar 

  4. Kelleher I, Harley M, Lynch F, Arseneault L, Fitzpatrick C, Cannon M (2008) Associations between childhood trauma, bullying and psychotic symptoms among a school-based adolescent sample. Br J Psychiatry J Ment Sci 193(5):378–382. https://doi.org/10.1192/bjp.bp.108.049536

    Article  Google Scholar 

  5. Borghans B, Homberg JR (2015) Animal models for posttraumatic stress disorder: an overview of what is used in research. World J Psychiatry 5(4):387–396. https://doi.org/10.5498/wjp.v5.i4.387

    Article  PubMed  PubMed Central  Google Scholar 

  6. Tamashiro KL, Nguyen MM, Sakai RR (2005) Social stress: from rodents to primates. Front Neuroendocrinol 26(1):27–40. https://doi.org/10.1016/j.yfrne.2005.03.001

    Article  PubMed  Google Scholar 

  7. Huhman KL (2006) Social conflict models: can they inform us about human psychopathology? Horm Behav 50(4):640–646. https://doi.org/10.1016/j.yhbeh.2006.06.022

    Article  PubMed  Google Scholar 

  8. Krishnan V (2014) Defeating the fear: new insights into the neurobiology of stress susceptibility. Exp Neurol 261:412–416. https://doi.org/10.1016/j.expneurol.2014.05.012

    Article  CAS  PubMed  Google Scholar 

  9. Kudryavtseva NN, Bakshtanovskaya IV, Koryakina LA (1991) Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav 38(2):315–320

    Article  CAS  Google Scholar 

  10. Toth I, Neumann ID (2013) Animal models of social avoidance and social fear. Cell Tissue Res 354(1):107–118. https://doi.org/10.1007/s00441-013-1636-4

    Article  PubMed  Google Scholar 

  11. Chaouloff F (2013) Social stress models in depression research: what do they tell us? Cell Tissue Res 354(1):179–190. https://doi.org/10.1007/s00441-013-1606-x

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hollis F, Kabbaj M (2014) Social defeat as an animal model for depression. ILAR J 55(2):221–232. https://doi.org/10.1093/ilar/ilu002

    Article  CAS  PubMed  Google Scholar 

  13. Altemus M (2006) Sex differences in depression and anxiety disorders: potential biological determinants. Horm Behav 50(4):534–538

    Article  Google Scholar 

  14. Breslau N, Davis GC, Andreski P, Peterson EL, Schultz LR (1997) Sex differences in posttraumatic stress disorder. Arch Gen Psychiatry 54(11):1044–1048

    Article  CAS  Google Scholar 

  15. Nolen-Hoeksema S (1987) Sex differences in unipolar depression: evidence and theory. Psychol Bull 101(2):259–282

    Article  CAS  Google Scholar 

  16. Weissman MM, Klerman GL (1977) Sex differences and the epidemiology of depression. Arch Gen Psychiatry 34(1):98–111

    Article  CAS  Google Scholar 

  17. St John RD, Corning PA (1973) Maternal aggression in mice. Behav Biol 9(5):635–639

    Article  CAS  Google Scholar 

  18. Hennessey AC, Huhman KL, Albers HE (1994) Vasopressin and sex differences in hamster flank marking. Physiol Behav 55(5):905–911

    Article  CAS  Google Scholar 

  19. Huhman KL, Solomon MB, Janicki M, Harmon AC, Lin SM, Israel JE, Jasnow AM (2003) Conditioned defeat in male and female Syrian hamsters. Horm Behav 44(3):293–299

    Article  Google Scholar 

  20. Taravosh-Lahn K, Delville Y (2004) Aggressive behavior in female golden hamsters: development and the effect of repeated social stress. Horm Behav 46(4):428–435. https://doi.org/10.1016/j.yhbeh.2004.03.007

    Article  PubMed  Google Scholar 

  21. Rosenhauer AM, McCann KE, Norvelle A, Huhman KL (2017) An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood. Horm Behav 93:31–38. https://doi.org/10.1016/j.yhbeh.2017.04.002

    Article  PubMed  Google Scholar 

  22. Faruzzi AN, Solomon MB, Demas GE, Huhman KL (2005) Gonadal hormones modulate the display of submissive behavior in socially defeated female Syrian hamsters. Horm Behav 47(5):569–575. https://doi.org/10.1016/j.yhbeh.2004.11.023

    Article  CAS  PubMed  Google Scholar 

  23. Solomon MB, Karom MC, Huhman KL (2007) Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters. Horm Behav 52(2):211–219. https://doi.org/10.1016/j.yhbeh.2007.04.007

    Article  CAS  PubMed  Google Scholar 

  24. Solomon MB, Karom MC, Norvelle A, Markham CA, Erwin WD, Huhman KL (2009) Gonadal hormones modulate the display of conditioned defeat in male Syrian hamsters. Horm Behav 56(4):423–428. https://doi.org/10.1016/j.yhbeh.2009.07.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. McCann KE, Rosenhauer AM, Jones GMF, Norvelle A, Choi DC, Huhman KL (2017) Histone deacetylase and acetyltransferase inhibitors modulate behavioral responses to social stress. Psychoneuroendocrinology 75:100–109. https://doi.org/10.1016/j.psyneuen.2016.10.022

    Article  CAS  PubMed  Google Scholar 

  26. Jasnow AM, Huhman KL (2001) Activation of GABA(A) receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters. Brain Res 920(1–2):142–150

    Article  CAS  Google Scholar 

  27. Markham CM, Taylor SL, Huhman KL (2010) Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learn Mem 17(2):109–116. https://doi.org/10.1101/lm.1633710

    Article  PubMed  PubMed Central  Google Scholar 

  28. Markham CM, Huhman KL (2008) Is the medial amygdala part of the neural circuit modulating conditioned defeat in Syrian hamsters? Learn Mem 15(1):6–12. https://doi.org/10.1101/lm.768208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jasnow AM, Shi C, Israel JE, Davis M, Huhman KL (2005) Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav Neurosci 119(4):1125–1130. https://doi.org/10.1037/0735-7044.119.4.1125

    Article  PubMed  Google Scholar 

  30. McCann KE, Sinkiewicz DM, Norvelle A, Huhman KL (2017) De novo assembly, annotation, and characterization of the whole brain transcriptome of male and female Syrian hamsters. Sci Rep 7:40472. https://doi.org/10.1038/srep40472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. De Vries GJ (2004) Minireview: Sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 145(3):1063–1068. https://doi.org/10.1210/en.2003-1504

    Article  CAS  PubMed  Google Scholar 

  32. de Vries GJ, Forger NG (2015) Sex differences in the brain: a whole body perspective. Biol Sex Differ 6:15. https://doi.org/10.1186/s13293-015-0032-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Marrocco J, Petty GH, Rios MB, Gray JD, Kogan JF, Waters EM, Schmidt EF, Lee FS et al (2017) A sexually dimorphic pre-stressed translational signature in CA3 pyramidal neurons of BDNF Val66Met mice. Nat Commun 8(1):808. https://doi.org/10.1038/s41467-017-01014-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Labonte B, Engmann O, Purushothaman I, Menard C, Wang J, Tan C, Scarpa JR, Moy G et al (2017) Sex-specific transcriptional signatures in human depression. Nat Med 23(9):1102–1111. https://doi.org/10.1038/nm.4386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Mead AN, Stephens DN (2003) Involvement of AMPA receptor GluR2 subunits in stimulus-reward learning: evidence from glutamate receptor gria2 knock-out mice. J Neurosci 23(29):9500–9507

    Article  CAS  Google Scholar 

  36. Gray AL, Hyde TM, Deep-Soboslay A, Kleinman JE, Sodhi MS (2015) Sex differences in glutamate receptor gene expression in major depression and suicide. Mol Psychiatry 20(9):1057–1068. https://doi.org/10.1038/mp.2015.91

    Article  CAS  PubMed  Google Scholar 

  37. Gulinello M, Gong QH, Smith SS (2002) Progesterone withdrawal increases the alpha4 subunit of the GABA(A) receptor in male rats in association with anxiety and altered pharmacology—a comparison with female rats. Neuropharmacology 43(4):701–714

    Article  CAS  Google Scholar 

  38. Gulinello M, Orman R, Smith SS (2003) Sex differences in anxiety, sensorimotor gating and expression of the alpha4 subunit of the GABAA receptor in the amygdala after progesterone withdrawal. Eur J Neurosci 17(3):641–648

    Article  CAS  Google Scholar 

  39. Tripp A, Oh H, Guilloux JP, Martinowich K, Lewis DA, Sibille E (2012) Brain-derived neurotrophic factor signaling and subgenual anterior cingulate cortex dysfunction in major depressive disorder. Am J Psychiatry 169(11):1194–1202. https://doi.org/10.1176/appi.ajp.2012.12020248

    Article  PubMed  PubMed Central  Google Scholar 

  40. Ortiz JB, Taylor SB, Hoffman AN, Campbell AN, Lucas LR, Conrad CD (2015) Sex-specific impairment and recovery of spatial learning following the end of chronic unpredictable restraint stress: potential relevance of limbic GAD. Behav Brain Res 282:176–184. https://doi.org/10.1016/j.bbr.2014.12.051

    Article  PubMed  PubMed Central  Google Scholar 

  41. Feldblum S, Erlander MG, Tobin AJ (1993) Different distributions of GAD65 and GAD67 mRNAS suggest that the two glutamate decarboxylases play distinctive functional roles. J Neurosci Res 34(6):689–706. https://doi.org/10.1002/jnr.490340612

    Article  CAS  PubMed  Google Scholar 

  42. Bowers G, Cullinan WE, Herman JP (1998) Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. J Neurosci 18(15):5938–5947

    Article  CAS  Google Scholar 

  43. Morrison KE, Swallows CL, Cooper MA (2011) Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol Behav 104(2):283–290. https://doi.org/10.1016/j.physbeh.2011.02.033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Bernstein HG, Dobrowolny H, Schott BH, Gorny X, Becker V, Steiner J, Seidenbecher CI, Bogerts B (2013) Increased density of AKAP5-expressing neurons in the anterior cingulate cortex of subjects with bipolar disorder. J Psychiatr Res 47(6):699–705. https://doi.org/10.1016/j.jpsychires.2012.12.020

    Article  PubMed  Google Scholar 

  45. Qi XR, Zhao J, Liu J, Fang H, Swaab DF, Zhou JN (2015) Abnormal retinoid and TrkB signaling in the prefrontal cortex in mood disorders. Cereb Cortex 25(1):75–83. https://doi.org/10.1093/cercor/bht203

    Article  PubMed  Google Scholar 

  46. Zhou R, Niwa S, Guillaud L, Tong Y, Hirokawa N (2013) A molecular motor, KIF13A, controls anxiety by transporting the serotonin type 1A receptor. Cell Rep 3(2):509–519. https://doi.org/10.1016/j.celrep.2013.01.014

    Article  CAS  PubMed  Google Scholar 

  47. Soleimani L, Roder JC, Dennis JW, Lipina T (2008) Beta N-acetylglucosaminyltransferase V (Mgat5) deficiency reduces the depression-like phenotype in mice. Genes Brain Behav 7(3):334–343. https://doi.org/10.1111/j.1601-183X.2007.00358.x

    Article  CAS  PubMed  Google Scholar 

  48. Wingo AP, Almli LM, Stevens JJ, Klengel T, Uddin M, Li Y, Bustamante AC, Lori A et al (2015) DICER1 and microRNA regulation in post-traumatic stress disorder with comorbid depression. Nat Commun 6:10106. https://doi.org/10.1038/ncomms10106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Yamamoto A, Uchiyama K, Nara T, Nishimura N, Hayasaka M, Hanaoka K, Yamamoto T (2014) Structural abnormalities of corpus callosum and cortical axonal tracts accompanied by decreased anxiety-like behavior and lowered sociability in spock3-mutant mice. Dev Neurosci 36(5):381–395. https://doi.org/10.1159/000363101

    Article  CAS  PubMed  Google Scholar 

  50. Dias C, Feng J, Sun H, Shao NY, Mazei-Robison MS, Damez-Werno D, Scobie K, Bagot R et al (2014) Beta-catenin mediates stress resilience through Dicer1/microRNA regulation. Nature 516(7529):51–55. https://doi.org/10.1038/nature13976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Lee JY, Kwak M, Lee PC (2015) Impairment of social behavior and communication in mice lacking the Uba6-dependent ubiquitin activation system. Behav Brain Res 281:78–85. https://doi.org/10.1016/j.bbr.2014.12.019

    Article  CAS  PubMed  Google Scholar 

  52. Gray CL, Norvelle A, Larkin T, Huhman KL (2015) Dopamine in the nucleus accumbens modulates the memory of social defeat in Syrian hamsters (Mesocricetus auratus). Behav Brain Res 286:22–28. https://doi.org/10.1016/j.bbr.2015.02.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ross AP, Norvelle A, Choi DC, Walton JC, Albers HE, Huhman KL (2017) Social housing and social isolation: Impact on stress indices and energy balance in male and female Syrian hamsters (Mesocricetus auratus). Physiol Behav 177:264–269. https://doi.org/10.1016/j.physbeh.2017.05.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Potegal M, Huhman K, Moore T, Meyerhoff J (1993) Conditioned defeat in the Syrian golden hamster (Mesocricetus auratus). Behav Neural Biol 60(2):93–102

    Article  CAS  Google Scholar 

  55. Albers HE, Huhman KL, Meisel RL (2002) Hormonal basis of social conflict and communication. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Moss RL, Rubin RR (eds) Hormones, brain and behavior. Academic Press, San Diego, p 393–433

    Chapter  Google Scholar 

  56. McCann KE, Bicknese CN, Norvelle A, Huhman KL (2014) Effects of inescapable versus escapable social stress in Syrian hamsters: the importance of stressor duration versus escapability. Physiol Behav 129:25–29. https://doi.org/10.1016/j.physbeh.2014.02.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. McCann KE, Huhman KL (2012) The effect of escapable versus inescapable social defeat on conditioned defeat and social recognition in Syrian hamsters. Physiol Behav 105(2):493–497. https://doi.org/10.1016/j.physbeh.2011.09.009

    Article  CAS  PubMed  Google Scholar 

  58. Hodes GE, Pfau ML, Purushothaman I, Ahn HF, Golden SA, Christoffel DJ, Magida J, Brancato A et al (2015) Sex differences in nucleus accumbens transcriptome profiles associated with susceptibility versus resilience to subchronic variable stress. J Neurosci 35(50):16362–16376. https://doi.org/10.1523/jneurosci.1392-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bagot RC, Cates HM, Purushothaman I, Vialou V, Heller EA, Yieh L, LaBonte B, Pena CJ et al (2017) Ketamine and imipramine reverse transcriptional signatures of susceptibility and induce resilience-specific gene expression profiles. Biol Psychiatry 81(4):285–295. https://doi.org/10.1016/j.biopsych.2016.06.012

    Article  CAS  PubMed  Google Scholar 

  60. Feng J, Wilkinson M, Liu X, Purushothaman I, Ferguson D, Vialou V, Maze I, Shao N et al (2014) Chronic cocaine-regulated epigenomic changes in mouse nucleus accumbens. Genome Biol 15(4):R65. https://doi.org/10.1186/gb-2014-15-4-r65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Konczal M, Koteja P, Stuglik MT, Radwan J, Babik W (2014) Accuracy of allele frequency estimation using pooled RNA-Seq. Mol Ecol Resour 14(2):381–392. https://doi.org/10.1111/1755-0998.12186

    Article  CAS  PubMed  Google Scholar 

  62. Sarajlic S, Edirisinghe N, Lukinov Y, Walters M, Davis B, Faroux G (2016) Orion: discovery environmenT for HPC research and bridging XSEDE resources. Paper presented at the Proceedings of the XSEDE16 Conference on Diversity, Big Data, and Science at Scale, Miami, USA,

  63. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. https://doi.org/10.1038/nbt.1883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D et al (2013) De novo transcript sequence reconstruction from RNA-seq using the trinity platform for reference generation and analysis. Nat Protoc 8(8):1494–1512. https://doi.org/10.1038/nprot.2013.084

    Article  CAS  PubMed  Google Scholar 

  65. Feng NY, Fergus DJ, Bass AH (2015) Neural transcriptome reveals molecular mechanisms for temporal control of vocalization across multiple timescales. BMC Genomics 16:408. https://doi.org/10.1186/s12864-015-1577-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/s0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  67. UniProt C (2015) UniProt: a hub for protein information. Nucleic Acids Res 43(Database issue):D204–D212. https://doi.org/10.1093/nar/gku989

    Article  CAS  Google Scholar 

  68. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1):1–16. https://doi.org/10.1186/1471-2105-12-323

    Article  CAS  Google Scholar 

  69. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140. https://doi.org/10.1093/bioinformatics/btp616

    Article  CAS  PubMed  Google Scholar 

  70. Plaisier SB, Taschereau R, Wong JA, Graeber TG (2010) Rank-rank hypergeometric overlap: identification of statistically significant overlap between gene-expression signatures. Nucleic Acids Res 38(17):e169. https://doi.org/10.1093/nar/gkq636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Mi H, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8(8):1551–1566. https://doi.org/10.1038/nprot.2013.092

    Article  CAS  PubMed  Google Scholar 

  72. Mi H, Poudel S, Muruganujan A, Casagrande JT, Thomas PD (2016) PANTHER version 10: expanded protein families and functions, and analysis tools. Nucleic Acids Res 44(D1):D336–D342. https://doi.org/10.1093/nar/gkv1194

    Article  CAS  PubMed  Google Scholar 

  73. Mi H, Thomas P (2009) PANTHER pathway: an ontology-based pathway database coupled with data analysis tools. Methods Mol Biol 563:123–140. https://doi.org/10.1007/978-1-60761-175-2_7

    Article  CAS  PubMed  Google Scholar 

  74. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14. https://doi.org/10.1186/gb-2010-11-2-r14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Langfelder P, Zhang B, Horvath S (2008) Defining clusters from a hierarchical cluster tree: the dynamic tree cut package for R. Bioinformatics 24:719–720. https://doi.org/10.1093/bioinformatics/btm563

    Article  CAS  PubMed  Google Scholar 

  76. Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9(1):1–13. https://doi.org/10.1186/1471-2105-9-559

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge Dr. James C. Walton, Alisa Norvelle, M.S., and Georgia State University’s Research Solutions and High Performance Computing Group for their expert assistance. The authors would also like to thank Reed A. Gilbert, Atit A. Patel, and Dr. Brittany M. Thompson for their technical assistance. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or Georgia State University.

Funding

This project was supported by NIH RO1MH062044 to KLH, Georgia State University Brains and Behavior Seed Grant to KLH, Georgia State University Dissertation Grant to KEM, Brains and Behavior Fellowships to KEM, DMS, and AMR, Honeycutt Fellowships to KEM and AMR, and a Next Generation Postdoctoral Fellowship from the Center for Behavioral Neuroscience to LQB.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kim L. Huhman.

Ethics declarations

All procedures and protocols were approved by the Georgia State University Institutional Animal Care and Use Committee and are in accordance with the standards outlined in the National Institutes of Health Guide for Care and Use of Laboratory Animals.

Conflict of Interest

The authors declare they have no conflict of interest.

Electronic Supplementary Material

ESM 1

(PDF 1818 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McCann, K.E., Sinkiewicz, D.M., Rosenhauer, A.M. et al. Transcriptomic Analysis Reveals Sex-Dependent Expression Patterns in the Basolateral Amygdala of Dominant and Subordinate Animals After Acute Social Conflict. Mol Neurobiol 56, 3768–3779 (2019). https://doi.org/10.1007/s12035-018-1339-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-018-1339-7

Keywords

Navigation