Considering sex as a biological variable will be valuable for neuroscience research

Journal of Neuroscience

Volumn 36, Issue 47, 2016, Pages 11817-11822

  Shansky, Rebecca M ^a   Woolley, Catherine S ^b  

^a NORTHEASTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEX HORMONE;

ALZHEIMER DISEASE; ARTICLE; BRAIN BIOCHEMISTRY; COGNITION; HEALTH CARE POLICY; HUMAN; META ANALYSIS (TOPIC); NEUROSCIENCE; NONHUMAN; PAIN; PRECLINICAL STUDY; PRIORITY JOURNAL; PUBLIC HEALTH; SCHIZOPHRENIA; SEX; SEX DIFFERENCE; STRESS; ANIMAL; FEMALE; FINANCIAL MANAGEMENT; MALE; MEDICAL RESEARCH; METHODOLOGY; NATIONAL HEALTH ORGANIZATION; SEXUAL DEVELOPMENT; STANDARDS; UNITED STATES;

ANIMALS; BIOMEDICAL RESEARCH; FEMALE; HUMANS; MALE; NATIONAL INSTITUTES OF HEALTH (U.S.); NEUROSCIENCES; RESEARCH DESIGN; RESEARCH SUPPORT AS TOPIC; SEX CHARACTERISTICS; SEX FACTORS; UNITED STATES;

EID: 84997281853     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1390-16.2016     Document Type: Article

References (56)

1. Abel KM, Drake R, Goldstein JM (2010) Sex differences in schizophrenia. Int Rev Psychiatry 22:417–428. CrossRef Medline
2. Archer J (1975) Rodent sex differences in emotional and related behavior. Behav Biol 14:451–479. CrossRef Medline
3. Bangasser DA, Wiersielis KR, Khantsis S (2016) Sex differences in the locus coeruleus-norepinephrine system and its regulation by stress. Brain Res 1641:177–188. CrossRef Medline
4. Becker JB, Koob GF (2016) Sex differences in animal models: focus on addiction. Pharmacol Rev 68:242–263. CrossRef Medline
5. Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA, Hampson E, Herman JP, Marts S, Sadee W, Steiner M, Taylor J, Young E (2005) Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146:1650–1673. CrossRef Medline
6. Becker JB, Prendergast BJ, Liang JW (2016) Female rats are not more variable than male rats: a meta-analysis of neuroscience studies. Biol Sex Differ 7:34. CrossRef Medline
7. Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35:565–572. CrossRef Medline
8. Breslau N (2009) The epidemiology of trauma, PTSD, and other posttrauma disorders. Trauma Violence Abuse 10:198–210. CrossRef Medline
9. Cahill L, Aswad D (2015) Sex influences on the brain: an issue whose time has come. Neuron 88:1084–1085. CrossRef Medline
10. Carrier N, Kabbaj M (2013) Sex differences in the antidepressant-like effects of ketamine. Neuropharmacology 70:27–34. CrossRef Medline
11. Castle D, Sham P, Murray R (1998) Differences in distribution of ages of onset in males and females with schizophrenia. Schizophr Res 33:179–183. CrossRef Medline
12. Christensen DL, Baio J, Van Naarden Braun K, Bilder D, Charles J, Constantino JN, Daniels J, Durkin MS, Fitzgerald RT, Kurzius-Spencer M, Lee LC, Pettygrove S, Robinson C, Schulz E, Wells C, Wingate MS, Zahorodny W, Yeargin-Allsopp M (2016) Prevalence and characteristics of autism spectrum disorder among children aged 8 years: autism and developmental disabilities monitoring network, 11 Sites, United States, 2012.MMWR Surveill Summ 65:1–23. CrossRef Medline
13. Clayton JA (2016) Studying both sexes: a guiding principle for biomedicine. FASEB J 30:519–524. CrossRef Medline
14. Clayton JA, Collins FS (2014) Policy: NIH to balance sex in cell and animal studies. Nature 509:282–283. CrossRef Medline
15. Dalla C, Antoniou K, Kokras N, Drossopoulou G, Papathanasiou G, Bekris S, Daskas S, Papadopoulou-Daifoti Z (2008) Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 93:595–605. CrossRef Medline
16. Dao DT, Mahon PB, Cai X, Kovacsics CE, Blackwell RA, Arad M, Shi J, Zandi PP, O’Donnell P, Knowles JA, Weissman MM, Coryell W, Scheftner WA, Lawson WB, Levinson DF, Thompson SM, Potash JB, Gould TD (2010) Mood disorder susceptibility gene CACNA1C modifies mood-related behaviors in mice and interacts with sex to influence behavior in mice and diagnosis in humans. Biol Psychiatry 68:801–810. CrossRef Medline
17. de Vries GJ (2004) Minireview. Sex differences in adult and developing brains: compensation, compensation, compensation. Endocrinology 145: 1063–1068. CrossRef Medline
18. Eliot L (2011) The trouble with sex differences. Neuron 72:895–898. CrossRef Medline
19. Fernandes C, González MI, Wilson CA, File SE (1999) Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 64:731–738. CrossRef Medline
20. Fields RD (2014) NIH policy: mandate goes too far. Nature 510:340. CrossRef Medline
21. Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL 3rd (2009) Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain 10:447–485. CrossRef Medline
22. Flórez-Vargas O, Brass A, Karystianis G, Bramhall M, Stevens R, Cruickshank S, Nenadic G (2016) Bias in the reporting of sex and age in biomedical research on mouse models. Elife 5:e13615. CrossRef Medline
23. Fowler CJ (2015) The potential of inhibitors of endocannabinoid metabolism as anxiolytic and antidepressive drugs: a practical view. Eur Neuropsychopharmacol 25:749–762. CrossRef Medline
24. Franceschelli A, Sens J, Herchick S, Thelen C, Pitychoutis PM (2015) Sex differences in the rapid and the sustained antidepressant-like effects of ketamine in stress-naive and “depressed” mice exposed to chronic mild stress. Neuroscience 290:49–60. CrossRef Medline
25. Good M, Day M, Muir JL (1999) Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region. Eur J Neurosci 11:4476–4480. CrossRef Medline
26. Gruene TM, Flick K, Stefano A, Shea SD, Shansky RM (2015) Sexually divergent expression of active and passive conditioned fear responses in rats. Elife 4:e11352. CrossRef Medline
27. Häfner H, Riecher-Rössler A, An Der Heiden W, Maurer K, Fätkenheuer B, Löffler W (1993) Generating and testing a causal explanation of the gender difference in age at first onset of schizophrenia. Psychol Med 23:925–940. CrossRef Medline
28. Itoh Y, Arnold AP (2015) Are females more variable than males in gene expression? Meta-analysis of microarray datasets. Biol Sex Differ 6:18. CrossRef Medline
29. Joel D, McCarthy MM (2016) Incorporating sex as a biological variable in neuropsychiatric research: where are we now and where should we be? Neuropsychopharmacology. Advance online publication. Retrieved June 22, 2016. CrossRef Medline
30. Joel D, Berman Z, Tavor I, Wexler N, Gaber O, Stein Y, Shefi N, Pool J, Urchs S, Margulies DS, Liem F, Hänggi J, Jäncke L, Assaf Y (2015) Sex beyond the genitalia: the human brain mosaic. Proc Natl Acad Sci U S A 112: 15468–15473. CrossRef Medline
31. Klein SL, Schiebinger L, Stefanick ML, Cahill L, Danska J, de Vries GJ, Kibbe MR, McCarthy MM, Mogil JS, Woodruff TK, Zucker I (2015) Opinion: Sex inclusion in basic research drives discovery. Proc Natl Acad Sci U S A 112:5257–5258. CrossRef Medline
32. Lukas M, Neumann ID (2014) Social preference and maternal defeatinduced social avoidance in virgin female rats: sex differences in involvement of brain oxytocin and vasopressin. J Neurosci Methods 234:101–107. CrossRef Medline
33. Maney DL (2016) Perils and pitfalls of reporting sex differences. Philos Trans R Soc Lond B Biol Sci 371:20150119. CrossRef Medline
34. Maren S, De Oca B, Fanselow MS (1994) Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res 661: 25–34. CrossRef Medline
35. Mazure CM (2016) Our evolving science: studying the influence of sex in preclinical research. Biol Sex Differ 7:15. CrossRef Medline
36. McCarthy MM (2015) Incorporating sex as a variable in preclinical neuropsychiatric research. Schizophr Bull 41:1016–1020. CrossRef Medline
37. McCarthy MM (2016) Multifaceted origins of sex differences in the brain. Philos Trans R Soc Lond B Biol Sci 371:20150106. CrossRef Medline
38. McCarthy MM, Arnold AP, Ball GF, Blaustein JD, de Vries GJ (2012) Sex differences in the brain: the not so inconvenient truth. J Neurosci 32: 2241–2247. CrossRef Medline
39. McCullough LD, McCarthy MM, de Vries GJ (2014) NIH policy: status quo is also costly. Nature 510:340. CrossRef Medline
40. Mercer AA, Palarz KJ, Tabatadze N, Woolley CS, Raman IM (2016) Sex differences in cerebellar synaptic transmission and sex-specific responses to autism-linked Gabrb3 mutations in mice. Elife 5:e07596. CrossRef Medline
41. Mogil JS (2012) Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat Rev Neurosci 13:859–866. CrossRef Medline
42. Mogil JS (2016) Perspective: equality need not be painful. Nature 535:S7. CrossRef Medline
43. Mogil JS, Chanda ML (2005) The case for the inclusion of female subjects in basic science studies of pain. Pain 117:1–5. CrossRef Medline
44. Panzica G, Melcangi RC (2016) Structural and molecular brain sexual differences: a tool to understand sex differences in health and disease. Neurosci Biobehav Rev 67:2–8. CrossRef Medline
45. Prendergast BJ, Onishi KG, Zucker I (2014) Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev 40:1–5. CrossRef Medline
46. Richardson SS, Reiches M, Shattuck-Heidorn H, LaBonte ML, Consoli T (2015) Opinion: focus on preclinical sex differences will not address women’s and men’s health disparities. Proc Natl Acad Sci U S A 112: 13419–13420. CrossRef Medline
47. Sanchis-Segura C, Becker JB (2016) Why we should consider sex (and study sex differences) in addiction research. Addict Biol 21:995–1006. CrossRef Medline
48. Shansky RM (2015) Sex differences in PTSD resilience and susceptibility: challenges for animal models of fear learning. Neurobiol Stress 1:60–65. CrossRef Medline
49. Shansky RM, Glavis-Bloom C, Lerman D, McRae P, Benson C, Miller K, Cosand L, Horvath TL, Arnsten AF (2004) Estrogen mediates sex differ- ences in stress-induced prefrontal cortex dysfunction. Mol Psychiatry 9:531–538. CrossRef Medline
50. Sorge RE, Mapplebeck JC, Rosen S, Beggs S, Taves S, Alexander JK, Martin LJ, Austin JS, Sotocinal SG, Chen D, Yang M, Shi XQ, Huang H, Pillon NJ, Bilan PJ, Tu Y, Klip A, Ji RR, Zhang J, Salter MW, et al. (2015) Different immune cells mediate mechanical pain hypersensitivity in male and female mice. Nat Neurosci 18:1081–1083. CrossRef Medline
51. Tabatadze N, Huang G, May RM, Jain A, Woolley CS (2015) Sex differences in molecular signaling at inhibitory synapses in the hippocampus. J Neurosci 35:11252–11265. CrossRef Medline
52. Tannenbaum C, Schwarz JM, Clayton JA, de Vries GJ, Sullivan C (2016) Evaluating sex as a biological variable in preclinical research: the devil in the details. Biol Sex Differ 7:13. CrossRef Medline
53. Tschanz JT, Corcoran CD, Schwartz S, Treiber K, Green RC, Norton MC, Mielke MM, Piercy K, Steinberg M, Rabins PV, Leoutsakos JM, Welsh- Bohmer KA, Breitner JC, Lyketsos CG (2011) Progression of cognitive, functional, and neuropsychiatric symptom domains in a population cohort with Alzheimer dementia: the Cache County Dementia Progression study. Am J Geriatr Psychiatry 19:532–542. CrossRef Medline
54. Warren SG, Humphreys AG, Juraska JM, Greenough WT (1995) LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res 703:26–30. CrossRef Medline
55. Yoon DY, Mansukhani NA, Stubbs VC, Helenowski IB, Woodruff TK, Kibbe MR (2014) Sex bias exists in basic science and translational surgical research. Surgery 156:508–516. CrossRef Medline
56. Zanos P, Moaddel R, Morris PJ, Georgiou P, Fischell J, Elmer GI, Alkondon M, Yuan P, Pribut HJ, Singh NS, Dossou KS, Fang Y, Huang XP, Mayo CL, Wainer IW, Albuquerque EX, Thompson SM, Thomas CJ, Zarate CA Jr, Gould TD (2016) NMDAR inhibition-independent antidepressant actions of ketamine metabolites. Nature 533:481–486. CrossRef Medline