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Research ArticleNew Research, Development

Pubertal Testosterone Programs Adult Behavioral Adaptations to Sexual Experience through Infralimbic Cortex ΔFosB

Kayla C. De Lorme, Nancy A. Staffend-Michael, Sarah C. Simmons, Alfred J. Robison and Cheryl L. Sisk
eNeuro 28 May 2019, 6 (3) ENEURO.0176-19.2019; DOI: https://doi.org/10.1523/ENEURO.0176-19.2019
Kayla C. De Lorme
1Department of Psychology, Michigan State University, East Lansing, MI 48824
4Department of Psychological Science, Gustavus Adolphus College, Saint Peter, MN 56082
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Nancy A. Staffend-Michael
2Neuroscience Program, Michigan State University, East Lansing, MI 48824
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Sarah C. Simmons
2Neuroscience Program, Michigan State University, East Lansing, MI 48824
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Alfred J. Robison
2Neuroscience Program, Michigan State University, East Lansing, MI 48824
3Department of Physiology, Michigan State University, East Lansing, MI 48824
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Cheryl L. Sisk
1Department of Psychology, Michigan State University, East Lansing, MI 48824
2Neuroscience Program, Michigan State University, East Lansing, MI 48824
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  • Figure 1.
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    Figure 1.

    Experimental design of experiment 1. T@P and sham-T@P males arrived four weeks before NoT@P and sham-NoT@P males to control for the age of shipping and environment during puberty. Two to 7 d after the NoT@P and sham-NoT@P arrived, males were either GDX or sham-GDX during adulthood (P56; T@P and sham-T@P) or prepubertally (P28; NoT@P and sham-NoT@P). Four weeks later, T@P and NoT@P males received testosterone (T)-filled capsules and sham males received empty (blank) capsules of the same size. Sexual behavior testing began two weeks later.

  • Figure 2.
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    Figure 2.

    Rate of ectopic mounting is dependent on pubertal testosterone. T@P males had significantly fewer ectopic mounts per minute compared to NoT@P males. Bars represent mean (±SEM); numbers on bars indicate sample size. *Main effect of pubertal testosterone, p ≤ 0.05.

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    Figure 3.

    The effects of pubertal testosterone and sexual experience on latency to mount, intromit, and ejaculate and number of intromissions to ejaculation. Mount latency: there was a main effect (ME) of sexual experience on mount latency with sexually experienced males having shorter latencies to mount compared to sexually naive males. Intromission latency: There was an ME of sexual experience on intromission latency with sexually experienced males having shorter latencies to intromit compared to sexually naive males. Ejaculation latency: there was a pubertal testosterone × sexual experience interaction on ejaculation latency with sexually naive NoT@P males having a longer latency to ejaculate compared to sexually naive T@P males. This effect was not seen in sexually experienced males. Intromissions to ejaculate: there was an ME of sexual experience for intromissions to ejaculate with sexually experienced males having less intromissions to achieve ejaculation compared to sexually naive males. Bars represent mean (±SEM); numbers on bars indicate sample size. +Interaction between pubertal testosterone and sexual experience, p ≤ 0.05.

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    Figure 4.

    Number of ΔFosB-ir cells in IL is dependent on pubertal testosterone and sexual experience. A, Brain atlas (Morin and Wood, 2001) representation of a coronal section containing the mPfC. B, Photomicrographs of drawn contours of the mPfC onto immunohistochemically-treated tissue sections at 4× objective. The mPfC included the anterior Cg1, PrL, and IL cortices; scale bar = 250 µm. C, The 2 × 2 panel of photomicrographs below the bar graph are representative images of ΔFosB-ir in the IL for the specified group of males; scale bars = 25 µm. D, In the CgL and PrL, there were no effects or interactions of pubertal testosterone and sexual experience on ΔFosB-ir cells, respectively. In the IL, there was an interaction between pubertal testosterone and sexual experience on ΔFosB-ir cells with sexual experienced T@P males having significantly more ΔFosB-ir cells compared to sexually naive T@P males. There were no significant differences in ΔFosB-ir cells as a function of sexual experience within NoT@P males. Bars represent mean (±SEM); numbers on bars indicate sample size. +Interaction between pubertal testosterone and sexual experience, p ≤ 0.05.

  • Figure 5.
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    Figure 5.

    Number of ΔFosB-ir cells in the NAc core and shell is dependent on pubertal testosterone and sexual experience. A, Brain atlas (Morin and Wood, 2001) representation of a coronal section containing the NAc. B, Photomicrographs of drawn contours of the NAc onto immunohistochemically-treated tissue sections. The NAc included the shell and core. LV = lateral ventricle; ac = anterior commissure. Scale bar = 250 µm. C, In the core, there was an interaction between pubertal testosterone and sexual experience on ΔFosB-ir cells with sexual experienced T@P males having significantly more ΔFosB-ir cells compared to sexually naive T@P males. There were no significant differences in ΔFosB-ir cells as a function of sexual experience within NoT@P males. In the shell, there was a main effect (ME) of sexual experience on ΔFosB-ir cells with sexually experienced males having more ΔFosB-ir expression compared to sexually naive males. Bars represent mean (±SEM); numbers on bars indicate sample sizes. +Interaction between pubertal testosterone and sexual experience, p ≤ 0.05.

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    Figure 6.

    Visualization of GFP to verify injection site and extent of infected cells in the IL. A, Boxes of representative injection sites in the IL for NoT@P-ΔFosB males over coronal atlas diagram (Morin and Wood, 2001). B, Photomicrograph of GFP overexpression in a NoT@P-ΔFosB male; scale bar = 250 µm. C, Photomicrograph of GFP overexpression in a NoT@P-ΔFosB male; scale bar = 100 µm.

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    Figure 7.

    Overexpression of ΔFosB in the IL decreases the rate of ectopic mounting in NoT@P males. NoT@P-ΔFosB males (n = 6) had significantly less ectopic mounts per minute compared to NoT@P-GFP males (n = 9). T@P-GFP males (n = 7) did not differ from either group in rate of ectopic mounting. Bars represent mean (±SEM). *Main effect of experimental group, p ≤ 0.05.

  • Figure 8.
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    Figure 8.

    The effects of ΔFosB overexpression in the IL and sexual experience on latency to mount, intromit, and ejaculate and number of intromissions to ejaculation. For mount latency, there was a pubertal testosterone × sexual experience interaction with sexually naive NoT@P-ΔFosB males having a longer latency to mount compared to sexually experienced NoT@P-ΔFosB males. This effect of sexual experience was not found in T@P-GFP or NoT@P-GFP males. For intromission latency and ejaculation latency, there was a main effect of sexual experience with sexually experienced males having shorter latencies to mount and intromit compared to sexually naive males. For intromissions to ejaculate, there was a main effect (ME) of sexual experience with sexually experienced males having less intromissions to achieve ejaculation compared to sexually naive males. Bars represent mean (±SEM); numbers on bars indicate sample size. +Interaction between experimental group and sexual experience, p ≤ 0.05.

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    Figure 9.

    Both sexual experience and ΔFosB increase dendritic spines in vmPFC. A, AAV-GFP was injected into the IL of naive (n = 22) or sexually experienced (n = 21) males, and AAV-GFP-ΔFosB was injected into the IL of naive males (n = 22). Immunofluorescence using a GFP antibody reveals spines of IL pyramidal neurons in all three groups. B, Thin spine density was increased by ΔFosB overexpression. Stubby spine density was not affected by either sexual experience nor ΔFosB overexpression. Mushroom spine density increased with sexual experience and showed a trend to increase by ΔFosB overexpression. Overall, total spine density was increased by ΔFosB overexpression. Bars represent mean (±SEM). *Main effect of experimental group, p < 0.05.

Tables

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    Table 1.

    Concentrations of plasma testosterone

    Plasma testosterone (ng/ml)
    GroupSexual experience
    NaiveExperienced
    T@P2.77 ± 1.013.54 ± 1.66
    NoT@P2.77 ± 1.213.68 ± 1.30
    Sham-T@P1.71 ± 0.722.59 ± 0.78
    Sham-NoT@P1.67 ± 0.882.57 ± 0.72
    • View popup
    Table 2.

    Statistics for sham controls

    FigureIndependent variable(s)Dependent variableStatistics (*significant)
    NASexual experienceLatency to mountF(1,24) = 14.65; p = 0.001*
     Latency to intromitF(1,24) = 14.33; p = 0.001*
     Latency to ejaculateF(1,24) = 31.27; p = 0.001*
     Intromissions to ejaculationF(1,17) = 12.24; p = 0.003*
      ΔFosB in the ILF(1,23) = 4.45; p = 0.046*
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    Table 3.

    Statistics for experiment 1

    FigureIndependent variable(s)Dependent variableStatistics (*significant)Post hoc comparison (if appropriate)Post hoc statistics (*significant)
    2Pubertal testosteroneEctopic mountingF(1,27) = 6.75; p = 0.015*  
     Sexual experienceF(1,27) = 0.69; p > 0.05 
     Pubertal testosterone × sexual experience F(1,27) = 0.54; p > 0.05  
    3Pubertal testosteroneLatency to mountF(1,27) = 0.272; p > 0.05  
     Sexual experienceF(1,27) = 17.43; p < 0.001* 
     Pubertal testosterone × sexual experience F(1,27) = 0.309; p > 0.05  
     Pubertal testosteroneLatency to intromitF(1,27) = 1.01; p > 0.05  
     Sexual experienceF(1,27) = 15.84; p < 0.001* 
     Pubertal testosterone × sexual experience F(1,27) = 2.50; p > 0.05  
     Pubertal testosterone × sexual experienceLatency to ejaculateF(1,27) = 12.70; p = 0.001*Pubertal testosterone in naive malesF(1,24) = 10.33; p = 0.004*
        Pubertal testosterone in experienced malesF(1,27) = 0.641; p > 0.05
     Pubertal testosteroneIntromissions to ejaculationF(1,26) = 0.465; p > 0.05  
     Sexual experienceF(1,26) = 25.00; p < 0.001* 
     Pubertal testosterone × sexual experienceF(1,26) = 2.73; p > 0.05 
    4DPubertal testosterone × sexual experienceΔFosB in the ILF(1,23) = 10.86; p = 0.003*sexual experience in T@P malesF(1,12) = 14.06; p = 0.003*
        sexual experience in NoT@P malesF(1,11) = 0.721; p > 0.05
     Pubertal testosteroneΔFosB in the Cg1F(1,23) = 0.046; p > 0.05
     Sexual experienceF(1,23) = 0.082; p > 0.05 
     Pubertal testosterone × sexual experience F(1,23) = 0.66; p > 0.05  
     Pubertal testosteroneΔFosB in the PrLF(1,23) = 0.133; p > 0.05  
     Sexual experienceF(1,23) = 2.04; p > 0.05 
     Pubertal testosterone × sexual experience F(1,23) = 2.57; p > 0.05  
    5CPubertal testosterone × sexual experienceΔFosB in the NAc coreF(1,23) = 5.42; p = 0.029*Sexual experience in T@P malesF(1,12) = 9.66; p = 0.009*
        Sexual experience in NoT@P malesF(1,11) = 0.042; p > 0.05
     Pubertal testosteroneΔFosB in the NAc shellF(1,23) = 1.60; p > 0.05  
     Sexual experienceF(1,23) = 7.041; p = 0.014* 
     Pubertal testosterone × sexual experience F(1,23) = 2.68; p > 0.05  
    • View popup
    Table 4.

    Statistics for experiment 2

    FigureIndependent variable(s)Dependent variableStatistics (*significant)Post hoc comparison (if appropriate)Post hoc statistics (*significant)
    7ΔFosB overexpressionEctopic mountingF(2,22) = 3.94; p = 0.035*NoT@P-ΔFosB vs NoT@P-GFP malesp = 0.043*
     Sexual experienceF(1,21) = 1.25; p > 0.05 
     ΔFosB overexpression × sexual experience F(1,21) = 1.20; p > 0.05  
    8ΔFosB overexpression × sexual experienceLatency to mountF(2,19) = 3.61; p = 0.047*Sexual experience in NoT@P-ΔFosB malesF(1,6) = 11.00; p = 0.015*
     Sexual experience in T@P-GFP malesF(1,6) = 1.61; p > 0.05
        Sexual experience in NoT@P-GFP malesF(1,7) = 0.61; p > 0.05
     ΔFosB overexpressionLatency to intromitF(2,20) = 1.12; p > 0.05  
     Sexual experienceF(1,20) = 14.09; p = 0.001* 
     ΔFosB overexpression × sexual experience F(2,20) = 3.06; p > 0.05  
     ΔFosB overexpressionLatency to ejaculateF(2,20) = 2.23; p > 0.05  
     Sexual experienceF(1,21) = 15.20; p < 0.001* 
     ΔFosB overexpression × sexual experience F(2,20) = 1.64; p > 0.05  
     ΔFosB overexpressionIntromissions to ejaculationF(2,21) = 0.87; p > 0.05  
     Sexual experienceF(1,20) = 11.70; p = 0.003* 
     ΔFosB overexpression × sexual experience F(2,20) = 0.06; p > 0.05  
    • View popup
    Table 5.

    Statistics for experiment 3

    FigureIndependent variable(s)Dependent variableStatistics (*significant)Post hoc comparison (if appropriate)Post hoc statistics (*significant)
    9BExperimental group (naive-GFP, experienced-GFP, naive-ΔFosB )Thin spinesF(2,62) = 1.717; p < 0.001*Naive-ΔFosB vs naive-GFP malesp < 0.001*
        Naive-ΔFosB vs experienced-GFP malesp = 0.016*
     Experimental group (naive-GFP, experienced-GFP, naive-ΔFosB )Stubby spinesF(2,62) = 0.723; p > 0.05  
     Experimental group (naive-GFP, experienced-GFP, naive-ΔFosB )Mushroom spinesF(2,61) = 4.080; p = 0.022*Naive-GFP vs experienced-GFP malesp = 0.029*
     Experimental group (naive-GFP, experienced-GFP, naive-ΔFosB )Total spinesF(2,62) = 9.359; p < 0.001*Naive-ΔFosB vs naive-GFP malesp < 0.001*
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Pubertal Testosterone Programs Adult Behavioral Adaptations to Sexual Experience through Infralimbic Cortex ΔFosB
Kayla C. De Lorme, Nancy A. Staffend-Michael, Sarah C. Simmons, Alfred J. Robison, Cheryl L. Sisk
eNeuro 28 May 2019, 6 (3) ENEURO.0176-19.2019; DOI: 10.1523/ENEURO.0176-19.2019

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Pubertal Testosterone Programs Adult Behavioral Adaptations to Sexual Experience through Infralimbic Cortex ΔFosB
Kayla C. De Lorme, Nancy A. Staffend-Michael, Sarah C. Simmons, Alfred J. Robison, Cheryl L. Sisk
eNeuro 28 May 2019, 6 (3) ENEURO.0176-19.2019; DOI: 10.1523/ENEURO.0176-19.2019
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Keywords

  • ΔFosB
  • ectopic mounts
  • medial prefrontal cortex
  • puberty
  • social proficiency
  • testosterone

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