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Articles, Behavioral/Cognitive

Pain Reduces Sexual Motivation in Female But Not Male Mice

Melissa A. Farmer, Alison Leja, Emily Foxen-Craft, Lindsey Chan, Leigh C. MacIntyre, Tina Niaki, Mengsha Chen, Josiane C.S. Mapplebeck, Vanessa Tabry, Lucas Topham, Melissa Sukosd, Yitzchak M. Binik, James G. Pfaus and Jeffrey S. Mogil
Journal of Neuroscience 23 April 2014, 34 (17) 5747-5753; https://doi.org/10.1523/JNEUROSCI.5337-13.2014
Melissa A. Farmer
1Department of Psychology and
2Alan Edwards Centre for Research on Pain, McGill University, Montréal, Quebec H3A 1B1, Canada, and
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Alison Leja
1Department of Psychology and
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Emily Foxen-Craft
1Department of Psychology and
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Lindsey Chan
1Department of Psychology and
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Leigh C. MacIntyre
1Department of Psychology and
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Tina Niaki
1Department of Psychology and
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Mengsha Chen
1Department of Psychology and
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Josiane C.S. Mapplebeck
1Department of Psychology and
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Vanessa Tabry
1Department of Psychology and
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Lucas Topham
1Department of Psychology and
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Melissa Sukosd
1Department of Psychology and
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Yitzchak M. Binik
1Department of Psychology and
2Alan Edwards Centre for Research on Pain, McGill University, Montréal, Quebec H3A 1B1, Canada, and
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James G. Pfaus
3Department of Psychology and Centre for Studies in Behavioral Neurobiology, Concordia University, Montréal, Quebec H4B 1R6, Canada
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Jeffrey S. Mogil
1Department of Psychology and
2Alan Edwards Centre for Research on Pain, McGill University, Montréal, Quebec H3A 1B1, Canada, and
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    Figure 1.

    Reduction of sexual behavior in female but not male mice by inflammatory pain. A, Decreased mounting behavior in a paced mating (F-PM) paradigm when female mice receive zymosan (ZYM) or carrageenan (CARR) injections to the vulva, hind paw, tail, or cheek, compared with uninjected female mice (No Inj.). Bars represent mean ± SEM mounts with (shaded) or without (open) intromissions; n = 7–12 mice/condition. B, Female mice with genital (vulvar; n = 6) or nongenital (combined hind paw, tail, and cheek; n = 23) pain spend less time on the side containing the male in a paced-mating chamber compared with mice receiving uninjected or vehicle injected mice (No Pain; n = 43). Bars represent mean ± SEM time on male side (s). C, No decreases in mounting behavior in an open field (M-OF) when male mice are treated similarly to female mice. Bars as in A; n = 6–10 mice/condition. D, No sex difference in mechanical allodynia produced by hind paw zymosan. Symbols represent mean ± SEM threshold (g) to withdraw from von Frey fibers before (BL) and after (Post-Inj.) bilateral zymosan injection; n = 6 mice/sex. E, No sex difference in facial grimacing produced by hind paw zymosan. Symbols represent mean ± SEM Mouse Grimace Scale (MGS) score before (BL) and after (Post-Inj.) bilateral zymosan injection; n = 4 mice/sex; *p < 0.05, **p < 0.01, ***p < 0.001 compared with vehicle (A, C), No Pain (B), or BL (D, E).

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    Figure 2.

    Reversal of hind paw carrageenan (CARR)-induced reduction in female sexual behavior (all F-PM) by the analgesic, pregabalin (PGB; A), and the libido-enhancing drugs apomorphine (APO; C) and melanotan-II (MT-II; E). The analgesic efficacy of PGB against was confirmed (B), as was the lack of effect on pain by APO (D) and MT-II (F). Bars in A, C, E represent mean ± SEM mounts with (shaded) or without (open) intromissions; n = 4–8 mice/condition. Symbols in B, D, F represent mean ± SEM Mouse Grimace Scale (MGS) score before carrageenan (BL), after carrageenan but before drug (CARR), and after drug (+PGB/+APO/+MT-II); n = 6–8 mice/drug; *p < 0.05, ***p < 0.001 compared with Veh/Veh group (A, C, E) or vehicle (B, D, F); •p < 0.05 compared with CARR/Veh group.

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    Table 1.

    Sexual behaviors affected by inflammatory pain in female mice in the paced mating (F-PM) paradigm

    ConditionnMount - I (no.)Mount + I (no.)Ejac. (no.)1st Mount (s)III (s)ID (s)M/I (no.)Crossings (s)Male side (s)Return (s)
    No treatment137.0 (2.1)33.5 (3.9)0.4 (0.1)609 (178)70 (10)12 (2)0.8 (0.04)43.4 (13.6)1962 (222)159 (61)
    Saline-vulva85.1 (1.4)24.4 (3.1)0.5 (0.2)1020 (238)79 (7)13 (1)0.8 (0.03)38.6 (8.4)1611 (317)210 (119)
    Saline-hind paw94.4 (1.3)32.3 (4.7)0.7 (0.2)293 (120)75 (12)12 (1)0.9 (0.04)41.0 (15.2)2090 (333)60 (19)
    Saline-tail710.1 (3.4)33.6 (6.3)0.3 (0.2)428 (175)60 (6)15 (3)0.8 (0.06)27.3 (11.2)1905 (302)90 (29)
    Saline-cheek712.1 (2.5)42.0 (8.3)0.3 (0.2)1245 (218)34 (7)9 (1)0.7 (0.11)14.0 (7.2)2721 (426)31 (20)
    No pain447.5 (1.0)32.8 (2.3)0.4 (0.1)691 (96)65 (5)12 (1)0.8 (0.02)34.8 (5.7)2036 (141)115 (31)
    ZYM-vulva (Genital pain)81.8 (0.4)**16.0 (2.8)**0.2 (0.2)765 (450)112 (26)22 (4)**0.9 (0.02)41.0 (15.1)1254 (375)*211 (114)
    ZYM-hind paw82.9 (0.8)18.2 (4.5)0.1 (0.1)1076 (315)133 (36)12 (1)0.9 (0.05)30.1 (11.4)1430 (397)392 (117)
    CARR-tail72.9 (1.1)12.0 (6.2)0.6 (0.2)582 (147)137 (58)17 (5)0.6 (0.14)40.6 (15.5)1025 (272)109 (39)
    CARR-cheek80.9 (0.6)5.8 (2.3)0 (0)602 (400)78 (34)7 (3)0.4 (0.19)15.4 (4.8)686 (191)377 (144)
    Nongenital pain232.2 (0.5)**12.0 (2.7)**0.2 (0.1)761 (181)116 (25)*12 (2)0.6 (0.08)*28.4 (6.5)1048 (179)**290 (68)*
    • Values represent mean (SEM). Mount - I, Frequency of mounts (defined as direct genital contact by the male onto flanks of the female without achieving penetration, often accompanied by female lordosis) without intromission; Mount + I, frequency mounts with intromission (defined as two or more distinct thrusts with penetration); Ejac., ejaculation frequency; 1st Mount, latency to first mount (with or without intromission); III, average inter-intromission interval; ID, average intromission duration; M/I, ratio of mounts to intromissions; Crossings, number of entries/exits into the male side; Male side, total time spent on male side; Return, average latency to return to the male side following intromission; CARR, carrageenan; ZYM, zymosan.

    • ↵*p < 0.05 compared with No Pain;

    • ↵**p < 0.01 compared with No Pain. ANOVAs were followed by Dunnett's case-comparison posthoc test with No Pain as the comparator group.

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    Table 2.

    Sexual behaviors not affected by inflammatory pain in male mice in the open field mating (M-OF) paradigm

    ConditionnMount - I (no.)Mount + I (no.)Ejac. (no.)1st Mount (s)III (s)ID (s)M/I (s)
    No treatment813.5 (5.1)45.4 (6.6)0 (0)432 (177)63 (10)11 (1)0.8 (0.05)
    Saline-penis712.9 (7.1)34.3 (5.9)0.4 (0.2)451 (331)82 (17)13 (1)0.8 (0.11)
    Saline-hind paw611.2 (4.7)43.0 (4.1)0.5 (0.2)195 (69)52 (6)11 (1)0.8 (0.06)
    Saline-tail75.1 (1.6)42.1 (8.1)0.3 (0.2)220 (75)78 (28)13 (2)0.7 (0.12)
    Saline-cheek834.0 (18.8)19.1 (4.1)0.8 (0.2)220 (67)85 (18)15 (1)0.5 (0.10)
    No pain3616.0 (4.7)36.4 (3.0)0.4 (0.1)314 (81)73 (8)13 (1)0.7 (0.04)
    ZYM-penis (Genital pain)1011.4 (3.5)22.0 (5.0)0.4 (0.2)540 (219)83 (23)12 (1)0.6 (0.10)
    ZYM-hind paw726.0 (9.5)33.1 (6.5)0.4 (0.2)168 (94)78 (14)11 (1)0.6 (0.13)
    CARR-tail810.1 (2.3)30.2 (4.7)0.6 (0.2)376 (76)103 (22)10 (1)0.8 (0.05)
    CARR-cheek722.7 (5.1)26.6 (6.4)0.8 (0.1)269 (43)103 (30)14 (1)0.5 (0.07)
    Nongenital pain2211.4 (3.5)30.0 (3.3)0.6 (0.1)282 (44)96 (13)11 (1)0.6 (0.05)
    • Values represent mean (SEM). Mount - I, Frequency of mounts (defined as direct genital contact by the male onto flanks of the female without achieving penetration, often accompanied by female lordosis) without intromission; Mount + I, frequency mounts with intromission (defined as two or more distinct thrusts with penetration); Ejac., ejaculation frequency; 1st Mount, latency to first mount (with or without intromission); III, average inter-intromission interval; ID, average intromission duration; M/I, ratio of mounts to intromissions; CARR, carrageenan; ZYM, zymosan.

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The Journal of Neuroscience: 34 (17)
Journal of Neuroscience
Vol. 34, Issue 17
23 Apr 2014
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Pain Reduces Sexual Motivation in Female But Not Male Mice
Melissa A. Farmer, Alison Leja, Emily Foxen-Craft, Lindsey Chan, Leigh C. MacIntyre, Tina Niaki, Mengsha Chen, Josiane C.S. Mapplebeck, Vanessa Tabry, Lucas Topham, Melissa Sukosd, Yitzchak M. Binik, James G. Pfaus, Jeffrey S. Mogil
Journal of Neuroscience 23 April 2014, 34 (17) 5747-5753; DOI: 10.1523/JNEUROSCI.5337-13.2014

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Pain Reduces Sexual Motivation in Female But Not Male Mice
Melissa A. Farmer, Alison Leja, Emily Foxen-Craft, Lindsey Chan, Leigh C. MacIntyre, Tina Niaki, Mengsha Chen, Josiane C.S. Mapplebeck, Vanessa Tabry, Lucas Topham, Melissa Sukosd, Yitzchak M. Binik, James G. Pfaus, Jeffrey S. Mogil
Journal of Neuroscience 23 April 2014, 34 (17) 5747-5753; DOI: 10.1523/JNEUROSCI.5337-13.2014
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Keywords

  • motivation
  • paced mating
  • pain
  • sex difference
  • sexual behavior

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