Front Integr Neurosci. 2018 Jul 19;12:29. doi: 10.3389/fnint.2018.00029. eCollection 2018.

Different Behavioral Experiences Produce Distinctive Parallel Changes in, and Correlate With, Frontal Cortex and Hippocampal Global Post-translational Histone Levels.

Frontiers in integrative neuroscience

Marissa Sobolewski, Garima Singh, Jay S Schneider, Deborah A Cory-Slechta

PMID: 30072878 PMCID: PMC6060276 DOI: 10.3389/fnint.2018.00029

Abstract

While it is clear that behavioral experience modulates epigenetic profiles, it is less evident how the nature of that experience influences outcomes and whether epigenetic/genetic "biomarkers" could be extracted to classify different types of behavioral experience. To begin to address this question, male and female mice were subjected to either a Fixed Interval (FI) schedule of food reward, or a single episode of forced swim followed by restraint stress, or no explicit behavioral experience after which global expression levels of two activating (H3K9ac and H3K4me3) and two repressive (H3K9me2 and H3k27me3) post-translational histone modifications (PTHMs), were measured in hippocampus (HIPP) and frontal cortex (FC). The specific nature of the behavioral experience differentiated profiles of PTHMs in a sex- and brain region-dependent manner, with all 4 PTHMs changing in parallel in response to different behavioral experiences. These different behavioral experiences also modified the pattern of correlations of PTHMs both within and across FC and HIPP. Unexpectedly, highly robust correlations were found between global PTHM levels and behavioral performances, suggesting that global PTHMs may provide a higher-order pattern recognition function. Further efforts are needed to determine the generality of such findings and what characteristics of behavioral experience are critical for modulating PTHM responses.

Keywords: FI schedule; behavior; epigenetics; forced swim; frontal cortex; global histone modification; hippocampus; restraint stress

References

1. Child Dev. 2015 Jan-Feb;86(1):303-9 - PubMed
2. Child Dev. 2013 Jan-Feb;84(1):49-57 - PubMed
3. JAMA Pediatr. 2015 Sep;169(9):822-9 - PubMed
4. Epigenetics. 2010 Aug 16;5(6):516-26 - PubMed
5. Neuroimage. 2014 Jan 1;84:245-53 - PubMed
6. BMC Cancer. 2017 Apr 12;17(1):261 - PubMed
7. Neuroscience. 2014 Nov 7;280:282-98 - PubMed
8. Neurotoxicology. 2016 May;54:65-71 - PubMed
9. Toxicol Sci. 2010 Oct;117(2):427-38 - PubMed
10. Environ Epigenet. 2016 Aug 08;2(3):dvw017 - PubMed
11. Neurosci Lett. 2004 Jan 9;354(2):169-71 - PubMed
12. Twin Res Hum Genet. 2015 Dec;18(6):623-34 - PubMed
13. Science. 2015 Jun 12;348(6240):1241-4 - PubMed
14. Prog Mol Biol Transl Sci. 2014;128:177-98 - PubMed
15. J Exp Anal Behav. 1972 Jul;18(1):155-67 - PubMed
16. Neuropsychopharmacology. 2010 Dec;35(13):2521-37 - PubMed
17. J Pharmacol Exp Ther. 1998 Aug;286(2):794-805 - PubMed
18. Stress. 2014 May;17(3):224-34 - PubMed
19. Eur Neuropsychopharmacol. 2013 Oct;23(10):1226-46 - PubMed
20. Proc Natl Acad Sci U S A. 2012 Apr 24;109(17):6490-5 - PubMed
21. Anat Sci Int. 2017 Jan;92(1):1-17 - PubMed
22. Transl Psychiatry. 2014 Apr 08;4:e381 - PubMed
23. J Neurosci. 2015 Dec 16;35(50):16362-76 - PubMed
24. Clin Epigenetics. 2016 Mar 31;8:34 - PubMed
25. Neuroimage. 2001 Dec;14(6):1290-301 - PubMed
26. Nat Commun. 2012;3:991 - PubMed
27. Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10604-9 - PubMed
28. Neurosci Lett. 2017 May 22;650:38-44 - PubMed
29. PLoS Comput Biol. 2011 Jan 06;7(1):e1001049 - PubMed
30. Exp Neurol. 2015 Jun;268:21-9 - PubMed
31. Neurosci Biobehav Rev. 2016 Dec;71:83-100 - PubMed
32. Hum Brain Mapp. 2017 Jun;38(6):3126-3140 - PubMed
33. Environ Health Perspect. 2004 May;112(6):717-30 - PubMed
34. Nat Neurosci. 2013 Oct;16(10):1445-52 - PubMed
35. J Am Acad Child Adolesc Psychiatry. 2014 Apr;53(4):417-24.e5 - PubMed
36. PLoS One. 2014 May 02;9(5):e94224 - PubMed
37. Anticancer Res. 2016 Aug;36(8):3961-4 - PubMed
38. Sci Transl Med. 2016 Aug 10;8(351):351ra106 - PubMed
39. J Neurochem. 2016 Oct;139 Suppl 2:179-199 - PubMed
40. Hippocampus. 2013 Jul;23(7):581-91 - PubMed
41. Neurotoxicology. 2014 Sep;44:169-83 - PubMed
42. Atten Percept Psychophys. 2018 Aug;80(6):1436-1448 - PubMed
43. Toxicol Appl Pharmacol. 1985 Apr;78(2):291-9 - PubMed
44. Am J Med Genet C Semin Med Genet. 2009 May 15;151C(2):136-41 - PubMed
45. J Neurosurg. 2013 Dec;119(6):1424-31 - PubMed
46. Science. 2014 Dec 12;346(6215):1256780 - PubMed
47. Nat Neurosci. 2015 Dec;18(12):1832-44 - PubMed
48. Epigenetics. 2009 Jan;4(1):47-53 - PubMed
49. Physiol Behav. 2016 Dec 1;167:313-323 - PubMed
50. Transl Behav Med. 2016 Mar;6(1):55-62 - PubMed
51. Nat Neurosci. 2015 May;18(5):773-8 - PubMed
52. Neuron. 2011 Jun 9;70(5):813-29 - PubMed
53. Clin Proteomics. 2014 Jun 03;11(1):24 - PubMed
54. Brain Res. 1997 Aug 1;764(1-2):253-6 - PubMed
55. Trauma Violence Abuse. 2006 Jan;7(1):34-60 - PubMed
56. Nat Neurosci. 2009 Mar;12(3):342-8 - PubMed
57. J Neurosci. 2004 Jun 16;24(24):5603-10 - PubMed
58. Front Behav Neurosci. 2015 Aug 21;9:221 - PubMed
59. Int J Epidemiol. 2012 Feb;41(1):62-74 - PubMed
60. Trends Genet. 2011 Oct;27(10):389-96 - PubMed
61. Neurotoxicol Teratol. 1996 Sep-Oct;18(5):565-75 - PubMed
62. PLoS One. 2014 Jan 24;9(1):e86822 - PubMed
63. J Neurosci. 2012 Oct 31;32(44):15626-42 - PubMed
64. Nat Rev Genet. 2001 May;2(5):383-7 - PubMed
65. Proc Natl Acad Sci U S A. 2016 Feb 2;113(5):1435-40 - PubMed
66. PLoS Comput Biol. 2011 May;7(5):e1002040 - PubMed
67. Brain Behav Immun. 2015 May;46:237-48 - PubMed
68. Biol Psychiatry. 2016 Jan 15;79(2):87-96 - PubMed
69. Front Neurosci. 2014 Sep 04;8:276 - PubMed
70. Insects. 2014 Jun 10;5(2):377-98 - PubMed

Publication Types

• Journal Article

Grant support

• P30 ES001247/ES/NIEHS NIH HHS/United States
• R01 ES021534/ES/NIEHS NIH HHS/United States