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Front Neurol. 2016 Jun 09;7:87. doi: 10.3389/fneur.2016.00087. eCollection 2016.

Sex Differences in Insular Cortex Gyri Responses to the Valsalva Maneuver.

Frontiers in neurology

Paul M Macey, Nicholas S Rieken, Rajesh Kumar, Jennifer A Ogren, Holly R Middlekauff, Paula Wu, Mary A Woo, Ronald M Harper

Affiliations

  1. UCLA School of Nursing, University of California at Los Angeles, Los Angeles, CA, USA; Brain Research Institute, University of California at Los Angeles, Los Angeles, CA, USA.
  2. UCLA School of Nursing, University of California at Los Angeles , Los Angeles, CA , USA.
  3. Brain Research Institute, University of California at Los Angeles, Los Angeles, CA, USA; Department of Anesthesiology, University of California at Los Angeles, Los Angeles, CA, USA; Department of Radiological Sciences, University of California at Los Angeles, Los Angeles, CA, USA.
  4. Department of Neurobiology, University of California at Los Angeles , Los Angeles, CA , USA.
  5. Department of Medicine, Division of Cardiology, David Geffen School of Medicine, University of California at Los Angeles , Los Angeles, CA , USA.
  6. Department of Neurobiology, University of California at Los Angeles, Los Angeles, CA, USA; Yale School of Medicine, Yale University, New Haven, CT, USA.
  7. Brain Research Institute, University of California at Los Angeles, Los Angeles, CA, USA; Department of Neurobiology, University of California at Los Angeles, Los Angeles, CA, USA.

PMID: 27375549 PMCID: PMC4899449 DOI: 10.3389/fneur.2016.00087

Abstract

Sex differences in autonomic regulation may underlie cardiovascular disease variations between females and males. One key autonomic brain region is the insular cortex, which typically consists of five main gyri in each hemisphere, and shows a topographical organization of autonomic function across those gyri. The present study aims to identify possible sex differences in organization of autonomic function in the insula. We studied brain functional magnetic resonance imaging (fMRI) responses to a series of four 18-s Valsalva maneuvers in 22 healthy females (age ± SD: 50.0 ± 7.9 years) and 36 healthy males (45.3 ± 9.2 years). Comparisons of heart rate (HR) and fMRI signals were performed with repeated measures ANOVA (threshold P < 0.05 for all findings). All subjects achieved the target 30 mmHg expiratory pressure for all challenges. Typical HR responses were elicited by the maneuver, including HR increases from ~4 s into the strain period (Phase II) and rapid declines to below baseline 5-10 s, following strain release (Phase IV). Small, but significant, sex differences in HR percent change occurred during the sympathetic-dominant Phase II (female < male) and parasympathetic-dominant Phase IV (female > male, i.e., greater undershoot in males). The insular cortices showed similar patterns in all gyri, with greater signal decreases in males than females. Both sexes exhibited an anterior-posterior topographical organization of insular responses during Phase II, with anterior gyri showing higher responses than more posterior gyri. The exception was the right anterior-most gyrus in females, which had lower responses than the four other right gyri. Responses were lateralized, with right-sided dominance during Phase II in both sexes, except the right anterior-most gyrus in females, which showed lower responses than the left. The findings confirm the anterior and right-sided sympathetic dominance of the insula. Although sex differences were prominent in response magnitude, organization differences between males and females were limited to the right anterior-most gyrus, which showed a lower fMRI response in females vs. males (and vs. other gyri in females). The sex differences suggest a possible differing baseline state of brain physiology or tonic functional activity between females and males, especially in the right anterior-most gyrus.

Keywords: autonomic; cardiovascular; fMRI; functional neuroanatomy; sympathetic

References

  1. Am J Physiol Regul Integr Comp Physiol. 2007 Feb;292(2):R788-93 - PubMed
  2. Int J Obes Relat Metab Disord. 1993 Aug;17(8):465-9 - PubMed
  3. Brain Res Bull. 1982 Feb;8(2):139-48 - PubMed
  4. Adv Tech Stand Neurosurg. 2004;29:265-88 - PubMed
  5. Clin Exp Pharmacol Physiol. 1999 Feb;26(2):122-6 - PubMed
  6. Neuroimage. 2003 Apr;18(4):880-94 - PubMed
  7. AJNR Am J Neuroradiol. 2004 Feb;25(2):222-32 - PubMed
  8. J Neurosci. 2013 Jun 19;33(25):10503-11 - PubMed
  9. Hypertension. 1993 Apr;21(4):498-503 - PubMed
  10. J Clin Neurophysiol. 1998 Nov;15(6):535-40 - PubMed
  11. J Nucl Med. 2016 Feb;57(2):221-5 - PubMed
  12. Am J Hypertens. 2009 Jul;22(7):723-9 - PubMed
  13. Clin Auton Res. 2015 Oct;25(5):317-26 - PubMed
  14. Brain Res. 2009 Oct 27;1295:119-26 - PubMed
  15. Aviat Space Environ Med. 1996 Apr;67(4):308-13 - PubMed
  16. Stereotact Funct Neurosurg. 2015;93(4):255-64 - PubMed
  17. Cardiovasc Res. 2002 Feb 15;53(3):678-87 - PubMed
  18. J Neurosci. 2009 Nov 11;29(45):14265-70 - PubMed
  19. Compr Physiol. 2016 Mar 15;6(2):1081-133 - PubMed
  20. Circulation. 2008 Jan 29;117(4):e25-146 - PubMed
  21. Cereb Cortex. 2008 Dec;18(12):2920-31 - PubMed
  22. Am J Physiol. 1998 May;274(5):R1417-24 - PubMed
  23. Neuroreport. 2004 Feb 9;15(2):357-61 - PubMed
  24. Hum Brain Mapp. 2014 Apr;35(4):1790-800 - PubMed
  25. J Neurosurg Anesthesiol. 2016 Apr;28(2):153-8 - PubMed
  26. J Comp Neurol. 1982 Nov 20;212(1):1-22 - PubMed
  27. Neuroscience. 2013 Apr 16;236:117-35 - PubMed
  28. Prog Neurobiol. 1998 Feb;54(2):149-68 - PubMed
  29. J Comp Neurol. 2014 Jan 1;522(1):64-97 - PubMed
  30. Neurol Clin. 1992 Feb;10(1):167-76 - PubMed
  31. Clin Sci Mol Med. 1978 Oct;55(4):321-7 - PubMed
  32. Environ Med. 2000 Dec;44(1):60-2 - PubMed
  33. Stroke. 2015 May;46(5):1196-201 - PubMed
  34. Neurosci Lett. 2009 Jun 26;457(2):66-70 - PubMed
  35. Neuroimage. 2007 Apr 1;35(2):698-708 - PubMed
  36. Clin Auton Res. 1996 Jun;6(3):131-40 - PubMed
  37. J Cogn Neurosci. 2007 Jul;19(7):1081-8 - PubMed
  38. J Comp Neurol. 2013 May 1;521(7):1598-613 - PubMed
  39. Brain Struct Funct. 2010 Jun;214(5-6):519-34 - PubMed
  40. Surg Radiol Anat. 2011 May;33(4):319-28 - PubMed
  41. Clin Neurol Neurosurg. 2013 Sep;115(9):1885-7 - PubMed
  42. Brain Res. 1998 Nov 30;813(1):73-81 - PubMed
  43. Am J Physiol. 1980 Nov;239(5):H581-93 - PubMed
  44. Neurosci Lett. 2013 Aug 26;548:217-21 - PubMed
  45. Auton Neurosci. 2009 May 11;147(1-2):56-63 - PubMed
  46. Circulation. 1994 Jul;90(1):583-612 - PubMed
  47. Neurology. 1992 Sep;42(9):1727-32 - PubMed
  48. J Comp Neurol. 2014 Jan 1;522(1):36-63 - PubMed
  49. Hum Brain Mapp. 2011 Oct;32(10):1592-601 - PubMed
  50. Ann Neurol. 2001 May;49(5):575-84 - PubMed
  51. Muscle Nerve. 1997 Dec;20(12):1561-8 - PubMed
  52. J Appl Physiol (1985). 2007 Oct;103(4):1402-11 - PubMed
  53. Acta Physiol Scand. 2000 Oct;170(2):111-8 - PubMed
  54. F1000Res. 2016 Apr 05;5:563 - PubMed
  55. Brain Res. 1990 Nov 12;533(1):66-72 - PubMed
  56. Respir Physiol. 2001 Feb;124(3):205-15 - PubMed
  57. Auton Neurosci. 2011 Feb 24;160(1-2):90-8 - PubMed
  58. JAMA. 1976 May 24;235(21):2299-306 - PubMed
  59. J Appl Physiol (1985). 1991 Oct;71(4):1563-7 - PubMed
  60. Clin Exp Hypertens. 1995 Jan-Feb;17(1-2):409-23 - PubMed
  61. Biol Psychiatry. 2007 Oct 15;62(8):847-55 - PubMed
  62. Acta Physiol (Oxf). 2016 Jun;217(2):103-19 - PubMed
  63. J Neuropsychiatry Clin Neurosci. 2014 Fall;26(4):276-82 - PubMed
  64. Am J Physiol. 1998 Aug;275(2):H689-96 - PubMed
  65. Am J Physiol. 1998 Nov;275(5):R1600-4 - PubMed
  66. J Anat. 1919 Jul;53(Pt 4):351-60 - PubMed
  67. J Auton Nerv Syst. 1989 Jul;27(2):165-72 - PubMed
  68. Front Hum Neurosci. 2013 Feb 04;7:14 - PubMed
  69. Acta Psychiatr Scand. 2013 Apr;127(4):269-78 - PubMed
  70. Nature. 1992 Sep 17;359(6392):181 - PubMed
  71. Neurosci Biobehav Rev. 2014 Feb;39:34-50 - PubMed
  72. Nurs Res. 1989 Nov-Dec;38(6):326-30 - PubMed
  73. Brain Res. 2004 Aug 20;1018(1):119-29 - PubMed
  74. J Am Soc Hypertens. 2010 Jul-Aug;4(4):174-82 - PubMed
  75. Circulation. 1991 Feb;83(2):484-91 - PubMed
  76. Neuroimage. 2002 May;16(1):217-40 - PubMed
  77. Pain. 2015 Jul;156(7):1232-9 - PubMed
  78. Brain Struct Funct. 2016 Jun;221(5):2695-701 - PubMed
  79. Pacing Clin Electrophysiol. 2014 Jul;37(7):884-8 - PubMed
  80. Science. 1982 Aug 13;217(4560):659-61 - PubMed
  81. Am Heart J. 1953 Feb;45(2):227-36 - PubMed
  82. Circulation. 1952 Jan;5(1):38-47 - PubMed
  83. Hypertension. 2005 Apr;45(4):522-5 - PubMed
  84. Front Psychiatry. 2016 Jan 21;7:3 - PubMed
  85. Brain Res. 1998 Jun 15;796(1-2):303-6 - PubMed
  86. J Cereb Blood Flow Metab. 1988 Dec;8(6):783-9 - PubMed
  87. J Comp Neurol. 1999 Nov 1;413(4):572-82 - PubMed
  88. Clin Auton Res. 2006 Feb;16(1):6-11 - PubMed
  89. Neuroimage. 2012 Aug 1;62(1):343-55 - PubMed
  90. J Cereb Blood Flow Metab. 2012 Jul;32(7):1188-206 - PubMed
  91. Front Neurosci. 2016 Jan 26;9:513 - PubMed
  92. BMC Psychiatry. 2015 Nov 18;15:295 - PubMed
  93. Nature. 2001 Jul 12;412(6843):150-7 - PubMed
  94. PLoS One. 2013 Oct 23;8(10):e76631 - PubMed
  95. J Neurosurg. 1999 Apr;90(4):720-33 - PubMed
  96. J Comp Neurol. 1987 Aug 1;262(1):27-45 - PubMed
  97. Stroke. 2009 Dec;40(12):e678-82 - PubMed
  98. Neuroreport. 2002 Dec 3;13(17):2371-4 - PubMed
  99. Heart. 2016 Jun 1;102(11):825-31 - PubMed
  100. J Neurosci. 2009 Feb 11;29(6):1817-25 - PubMed
  101. Can J Psychol. 1991 Dec;45(4):507-22 - PubMed
  102. Auton Neurosci. 2012 May 21;168(1-2):72-81 - PubMed
  103. Brain Struct Funct. 2011 Jun;216(2):137-49 - PubMed
  104. Cereb Cortex. 2006 Aug;16(8):1232-8 - PubMed
  105. Am J Cardiol. 1995 Nov 1;76(12):906-12 - PubMed
  106. Am J Physiol Regul Integr Comp Physiol. 2007 Feb;292(2):R715-22 - PubMed
  107. Clin Exp Pharmacol Physiol. 2007 Sep;34(9):827-32 - PubMed
  108. Surg Radiol Anat. 2003 May;25(2):113-9 - PubMed
  109. J Psychiatr Res. 2011 Aug;45(8):1027-35 - PubMed
  110. Prog Brain Res. 2010;186:3-12 - PubMed
  111. Prog Brain Res. 1982;57:267-77 - PubMed
  112. Arch Intern Med (Chic). 1947 Oct;80(4):454-62 - PubMed
  113. Int J Pediatr Otorhinolaryngol. 2015 Nov;79(11):1851-5 - PubMed
  114. Compr Physiol. 2014 Jul;4(3):1121-55 - PubMed
  115. Cereb Cortex. 2012 Sep;22(9):1979-92 - PubMed
  116. Acta Radiol. 2015 Feb;56(2):204-13 - PubMed
  117. J Appl Physiol (1985). 1994 Aug;77(2):606-13 - PubMed
  118. Depress Anxiety. 2009;26(5):480-91 - PubMed
  119. J Comp Neurol. 1991 Sep 1;311(1):1-16 - PubMed
  120. Brain Res. 1997 Jun 20;760(1-2):243-50 - PubMed
  121. Prog Brain Res. 2012;195:123-63 - PubMed
  122. Can J Physiol Pharmacol. 1998 Jul-Aug;76(7-8):737-46 - PubMed
  123. Clin Exp Pharmacol Physiol. 2016 Apr;43(4):484-93 - PubMed
  124. Hum Brain Mapp. 2006 Apr;27(4):314-24 - PubMed
  125. J Auton Nerv Syst. 1998 Nov 10;73(2-3):182-5 - PubMed
  126. Stroke. 1994 Jan;25(1):113-6 - PubMed
  127. Clin Auton Res. 2005 Aug;15(4):292-8 - PubMed

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