title: Pleiotropic Control by Testosterone of a Learned Vocal Behavior and Its Underlying Neuroplasticity(1,2,3).
abstract: Steroid hormones coordinate multiple aspects of behavior and physiology. The same hormone often regulates different aspects of a single behavior and its underlying neuroplasticity. This pleiotropic regulation of behavior and physiology is not well understood. Here, we investigated the orchestration by testosterone (T) of birdsong and its neural substrate, the song control system. Male canaries were castrated and received stereotaxic implants filled with T in select brain areas. Implanting T solely in the medial preoptic nucleus (POM) increased the motivation to sing, but did not enhance aspects of song quality such as acoustic structure and stereotypy. In birds implanted with T solely in HVC (proper name), a key sensorimotor region of the song control system, little or no song was observed, similar to castrates that received no T implants of any sort. However, implanting T in HVC and POM simultaneously rescued all measures of song quality. Song amplitude, though, was still lower than what was observed in birds receiving peripheral T treatment. T in POM enhanced HVC volume bilaterally, likely due to activity-dependent changes resulting from an enhanced song rate. T directly in HVC, without increasing song rate, enhanced HVC volume on the ipsilateral side only. T in HVC enhanced the incorporation and recruitment of new neurons into this nucleus, while singing activity can independently influence the incorporation of new neurons into HVC. These results have broad implications for how steroid hormones integrate across different brain regions to coordinate complex social behaviors.
authors.affiliation: Department of Psychological and Brain Sciences, The Johns Hopkins University, Baltimore, Maryland 21218; Department of Psychology, University of Maryland, College Park, Maryland 20742.
authors.forename: Beau A
authors.initials: BA
authors.lastname: Alward
authors.affiliation: Department of Psychological and Brain Sciences, The Johns Hopkins University, Baltimore, Maryland 21218; Department of Psychology, University of Maryland, College Park, Maryland 20742.
authors.forename: Farrah N
authors.initials: FN
authors.lastname: Madison
authors.affiliation: Department of Psychological and Brain Sciences, The Johns Hopkins University , Baltimore, Maryland 21218.
authors.forename: Shannon E
authors.initials: SE
authors.lastname: Parker
authors.affiliation: GIGA Neuroscience, University of Liège , 4000 Liège, Belgium.
authors.forename: Jacques
authors.identifier: 0000-0001-9492-2126
authors.initials: J
authors.lastname: Balthazart
authors.affiliation: Department of Psychological and Brain Sciences, The Johns Hopkins University, Baltimore, Maryland 21218; Department of Psychology, University of Maryland, College Park, Maryland 20742.
authors.forename: Gregory F
authors.identifier: 0000-0002-4784-0520
authors.initials: GF
authors.lastname: Ball
mesh_terms: D000818:Animals; D002171:Canaries; D053400:High Vocal Center / Q000187:drug effects / Q000502:physiology*; D008297:Male; D009473:Neuronal Plasticity; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D011301:Preoptic Area / Q000187:drug effects / Q000502:physiology*; D013018:Sound Spectrography; D013739:Testosterone / Q000008:administration & dosage / Q000502:physiology*; D014828:Vocalization, Animal / Q000187:drug effects / Q000502:physiology*
chemical_list: D013739:Testosterone
keywords: medial preoptic area; neurogenesis; singing behavior; social behavior; songbirds
references.citation: Gen Comp Endocrinol. 1977 Jan;31(1):72-4
references.pmid: 832820
references.citation: Dev Neurobiol. 2016 Jan;76(1):3-18
references.pmid: 25864444
references.citation: Physiol Behav. 1990 Nov;48(5):599-609
references.pmid: 2082358
references.citation: Horm Behav. 1988 Sep;22(3):402-18
references.pmid: 3169703
references.citation: J Exp Biol. 2012 Jan 15;215(Pt 2):201-9
references.pmid: 22189763
references.citation: Trends Neurosci. 2000 Jun;23(6):251-8
references.pmid: 10838594
references.citation: J Neurosci. 1995 Jun;15(6):4408-16
references.pmid: 7540674
references.citation: Anim Behav. 2009 Mar 1;77(3):701-706
references.pmid: 20161558
references.citation: J Neurosci. 2014 Dec 10;34(50):16821-34
references.pmid: 25505334
references.citation: J Comp Neurol. 1988 May 15;271(3):346-54
references.pmid: 3385013
references.citation: Gen Comp Endocrinol. 2015 Oct 1;222:150-7
references.pmid: 26391838
references.citation: J Neurosci. 2011 Jun 29;31(26):9649-57
references.pmid: 21715630
references.citation: ILAR J. 2009;50(1):5-14
references.pmid: 19106448
references.citation: Annu Rev Physiol. 1987;49:349-64
references.pmid: 3551805
references.citation: J Comp Neurol. 2014 Dec 15;522(18):4100-20
references.pmid: 25131458
references.citation: Front Neuroendocrinol. 2002 Apr;23(2):137-78
references.pmid: 11950243
references.citation: Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4756-61
references.pmid: 23449880
references.citation: Neuron. 2014 Apr 2;82(1):208-23
references.pmid: 24698276
references.citation: Horm Behav. 1976 Mar;7(1):105-38
references.pmid: 819345
references.citation: J Neurosci. 1994 Nov;14(11 Pt 2):6924-34
references.pmid: 7965088
references.citation: Gen Comp Endocrinol. 2004 Apr;136(2):192-9
references.pmid: 15028522
references.citation: Front Neuroendocrinol. 2015 Apr;37:119-28
references.pmid: 25285401
references.citation: Neuron. 1999 Jan;22(1):53-62
references.pmid: 10027289
references.citation: Science. 1996 Sep 27;273(5283):1871-5
references.pmid: 8791594
references.citation: J Neurobiol. 2002 May;51(2):129-41
references.pmid: 11932954
references.citation: Eur J Neurosci. 2004 Jan;19(2):234-46
references.pmid: 14725617
references.citation: Horm Behav. 2000 Dec;38(4):250-61
references.pmid: 11104643
references.citation: Annu Rev Neurosci. 1979;2:65-112
references.pmid: 395885
references.citation: J Physiol Sci. 2008 Aug;58(4):213-20
references.pmid: 18505601
references.citation: Neuroscience. 2006;138(3):939-46
references.pmid: 16310314
references.citation: Psychoneuroendocrinology. 1991;16(1-3):41-66
references.pmid: 1961844
references.citation: ILAR J. 2010;51(4):362-77
references.pmid: 21131713
references.citation: J Comp Neurol. 1992 Mar 22;317(4):407-20
references.pmid: 1578004
references.citation: Horm Behav. 2009 Jan;55(1):217-27
references.pmid: 19013173
references.citation: PLoS One. 2013;8(5):e63692
references.pmid: 23691086
references.citation: J Comp Neurol. 1976 Feb 15;165(4):457-86
references.pmid: 1262540
references.citation: Eur J Neurosci. 2008 Feb;27(4):801-17
references.pmid: 18333960
references.citation: Nature. 1998 Sep 3;395(6697):67-71
references.pmid: 12071206
references.citation: J Neurobiol. 1998 Sep 5;36(3):441-53
references.pmid: 9733078
references.citation: Science. 1981 Dec 18;214(4527):1368-70
references.pmid: 7313697
references.citation: Gen Comp Endocrinol. 2008 Aug;158(1):10-9
references.pmid: 18597755
references.citation: Horm Behav. 2008 Aug;54(3):347-54
references.pmid: 18539279
references.citation: J Comp Neurol. 1995 Oct 2;360(4):726-34
references.pmid: 8801262
references.citation: J Exp Biol. 2008 Jan;211(Pt 1):66-78
references.pmid: 18083734
references.citation: Gen Comp Endocrinol. 2008 Jul;157(3):259-65
references.pmid: 18457836
references.citation: J Comp Neurol. 1974 Aug 1;156(3):337-74
references.pmid: 4609173
references.citation: Brain Behav Evol. 2014;84(1):1-4
references.pmid: 25034511
references.citation: Horm Behav. 2008 Aug;54(3):373-8
references.pmid: 18571653
references.citation: J Neurobiol. 1986 Nov;17(6):605-12
references.pmid: 3794688
references.citation: J Exp Biol. 2009 Apr;212(Pt 8):1212-24
references.pmid: 19329754
references.citation: Eur J Neurosci. 2014 Sep;40(6):2941-7
references.pmid: 24974859
references.citation: Horm Behav. 1991 Sep;25(3):367-81
references.pmid: 1937428
references.citation: J Neurosci. 1997 Aug 1;17(15):6001-10
references.pmid: 9221796
references.citation: J Neurosci. 2007 Oct 31;27(44):12045-57
references.pmid: 17978046
references.citation: J Comp Neurol. 2004 May 31;473(3):377-414
references.pmid: 15116397
references.citation: Gen Comp Endocrinol. 1979 Mar;37(3):286-93
references.pmid: 456869
references.citation: Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8584-9
references.pmid: 10890902
references.citation: Behav Neural Biol. 1986 Nov;46(3):445-71
references.pmid: 3814048
references.citation: Horm Behav. 2014 Nov;66(5):731-42
references.pmid: 25308086
references.citation: J Comp Neurol. 1999 Aug 30;411(3):487-94
references.pmid: 10413781
references.citation: Nature. 2005 Feb 10;433(7026):638-43
references.pmid: 15703748
references.citation: Horm Behav. 2008 Sep;54(4):488-95
references.pmid: 18452920
references.citation: Ann N Y Acad Sci. 2004 Jun;1016:586-610
references.pmid: 15313796
references.citation: J Comp Neurol. 1976 Feb 15;165(4):487-511
references.pmid: 1262541
references.citation: J Neurobiol. 1997 Dec;33(7):865-76
references.pmid: 9407010
references.citation: Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12421-6
references.pmid: 12218180
references.citation: Brain Res. 1980 Jun 16;192(1):89-107
references.pmid: 7378793
references.citation: Gen Comp Endocrinol. 2015 May 1;215:61-75
references.pmid: 25260250
references.citation: J Neurobiol. 2003 Nov;57(2):130-40
references.pmid: 14556279
references.citation: J Chem Neuroanat. 2007 May;33(3):140-54
references.pmid: 17367992
references.citation: J Neurobiol. 1988 Oct;19(7):624-35
references.pmid: 3225559
references.citation: Anim Behav. 2000 Jun;59(6):1167-1176
references.pmid: 10877896
references.citation: J Comp Neurol. 1991 Jul 22;309(4):486-94
references.pmid: 1655832
references.citation: Brain Res. 1989 May 29;488(1-2):253-9
references.pmid: 2743120
references.citation: J Neurosci. 2002 Oct 1;22(19):8684-90
references.pmid: 12351743
references.citation: Annu Rev Neurosci. 2013 Jul 8;36:489-517
references.pmid: 23750515
references.citation: J Steroid Biochem Mol Biol. 1991 Aug;39(2):223-32
references.pmid: 1888681
references.citation: Neuroscience. 2003;121(3):801-14
references.pmid: 14568038
references.citation: J Comp Neurol. 1999 Apr 28;407(1):115-29
references.pmid: 10213192
references.citation: Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15520-5
references.pmid: 17875989
references.citation: Endocrinology. 1999 Oct;140(10):4633-43
references.pmid: 10499520
references.citation: Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19573-8
references.pmid: 24218603
references.citation: J Neurosci. 1984 Mar;4(3):786-92
references.pmid: 6707734