CoChat
Sign Up
Cited by 72Neuroendocrine regulation and behaviorSexual Differentiation and DisordersAutism Spectrum Disorder Research

Effects of sex and gonadectomy on social investigation and social recognition in mice

Open access
Karlsson, Sara A., Haziri, Kaltrina, Hansson, Evelyn, Kettunen, Petronella, Westberg, Lars·2015·BMC Neuroscience
DOI 10.1186/s12868-015-0221-zPMC PMC4660658
Open this paper in CoChat — free accountOpen PDF

Abstract

BACKGROUND: An individual's ability to recognise and pay attention to others is crucial in order to behave appropriately in various social situations. Studies in humans have shown a sex bias in sociability as well as social memory, indicating that females have better face memory and gaze more at the eyes of others, but information about the factors that underpin these differences is sparse. Our aim was therefore to investigate if sociability and social recognition differ between female and male mice, and if so, to what extent gonadal hormones may be involved. Intact and gonadectomised male and female mice were assessed for sociability and social recognition using the three-chambered sociability paradigm, as well as the social discrimination test. Furthermore, we conducted a novel object recognition test, a locomotor activity test and an odour habituation/dishabituation test. RESULTS: The present study showed that the ability to recognise other individuals is intact in males with and without gonads, as well as in intact females, whereas it is hampered in gonadectomised females. Additionally, intact male mice displayed more persistent investigatory behaviour compared to the other groups, although the intact females showed elevated basal locomotor activity. In addition, all groups had intact object memory and habituated to odours. CONCLUSIONS: Our results suggest that intact male mice investigate conspecifics more than females do, and these differences seem to depend upon circulating hormones released from the testis. As these results seem to contrast what is known from human studies, they should be taken into consideration when using the three-chambered apparatus, and similar paradigms as animal models of social deficits in e.g. autism. Other behavioural tests, and animal models, may be more suitable for translational studies between patients and experimental animals.

AI snapshot

Written from the paper’s full text.

TL;DR

In C57Bl/6N mice, intact males investigated conspecifics and novel objects more than females or gonadectomised males, and this difference appeared testis-dependent. Social recognition was intact in intact and gonadectomised males and intact females, but was hampered in gonadectomised females.

Key findings

  • Intact males spent significantly more time exploring stimulus animals than both female groups and gonadectomised (GDX) males in the social discrimination sampling session (between-group p < 0.001), and intact males also investigated stimulus mice longer than all other groups in the three-chambered test (p < 0.001).
  • Social recognition was present in intact males, GDX males, and intact females; GDX females showed only a tendency for significance on either social discrimination or social memory score. In the choice session, the two male groups spent more time investigating the novel mouse than the two female groups (p < 0.01).
  • All four groups showed sociability in the three-chambered apparatus (more time in the social chamber and more sniffing of the stimulus mouse, within-group p < 0.01), and all groups showed object recognition memory (within-group p < 0.01); intact males spent more time investigating the novel object than both female groups (p < 0.05).
  • Intact females showed elevated locomotor activity compared with the other groups (p < 0.01). All groups habituated to odours, and intact males investigated the social odour longer than both GDX groups (p < 0.01), with a trend versus intact females (p = 0.08). Plasma testosterone was 6.1 ± 0.6 ng/ml in males, 0.1 ± 0.1 ng/ml in females, 0.1 ± 0.1 ng/ml in GDX females, and 0.07 ± 0.3 ng/ml in GDX males.

Methods

  • Adult C57Bl/6N mice were used across experiments A–D. Experiment D compared four groups: intact males (n = 14), intact females (n = 14), GDX males (n = 14), and GDX females (n = 15); gonadectomy was performed 3 weeks before the study, and stimulus mice were GDX females.
  • Behavioural testing included the social discrimination test, three-chambered sociability test, novel object recognition test, locomotor activity/open field test, and olfactory habituation/dishabituation test. Plasma testosterone was measured by ELISA.
  • Statistical analysis used a linear mixed model in SAS 9.3 PROC MIXED; social and object recognition memory scores were analysed with one-sample t tests against a cut-off of 0.5 in SPSS, with p < 0.05 considered significant.

Limitations

  • The paper states that estrus cycle phase was not included, so its previously reported importance for social recognition could not be confirmed. It also states that long-term social recognition was not tested.
  • The paper notes that only GDX and intact females were used as stimulus animals, so the observed sex difference in social investigation could potentially depend on stimulus sex, although it cites prior findings arguing against this.
  • Evident from the text: the study used a single mouse strain and relatively modest group sizes, and scoring was performed by one trained observer, which may limit generalisability and independent verification.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1186/s12868-015-0221-z

Cites

45 of 45 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

14 of 48 cited sources checked · 9 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Male rodents lacking gonads, androgen receptors or estrogen receptors display substantially decreased aggression and sexual behaviours.

    “Male rodents lacking gonads, androgen receptors or estrogen receptors display substantially decreased aggression and sexual behaviours [8–11]”
    Quote in the paperSubstantial claim2 of 4 sources checked
    • cites [8] Sato T, Matsumoto T, Kawano H, Watanabe T, Uematsu Y, Sekine K, Fukuda T, Aihara K, Krust A, Yamada T, et al. Brain masculinization requires androgen receptor function. Proc Natl Acad Sci USA. 2004;101(6):1673–8. source
    • cites [9] Juntti SA, Tollkuhn J, Wu MV, Fraser EJ, Soderborg T, Tan S, Honda S, Harada N, Shah NM. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron. 2010;66(2):260–72. source

      The Discussion reports substantial deficits in mating and territorial behaviour in male mice lacking neural androgen receptors, and the Introduction reports loss of male sexual and aggressive behaviours in mice lacking both estrogen receptors. These passages concern mice rather than rodents generally. Our copy does not establish the claimed behavioural decrease in males lacking gonads. (LLM, conf=0.85)

      Experimental — accuracy not yet measured
    • cites [10] Raskin K, de Gendt K, Duittoz A, Liere P, Verhoeven G, Tronche F, Mhaouty-Kodja S. Conditional inactivation of androgen receptor gene in the nervous system: effects on male behavioral and neuroendocrine responses. J Neurosci Off J Soc Neurosci. 2009;29(14):4461–70. source

      The section “Sexual and aggressive behaviors of gonadectomized and T-treated mice” reports reduced sexual behavior and aggression in male mice lacking androgen receptors in the nervous system. It does not establish that loss of gonads or estrogen receptors likewise decreases both behaviors: the gonadectomized mice in this comparison received testosterone, and estrogen-receptor loss was not tested. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
    • cites [11] Pfaff D, Choleris E, Ogawa S, Ogawa S, Lubahn DB, Korach KS, Pfaff DW. Genes for sex hormone receptors controlling mouse aggression Behavioral effects of estrogen receptor gene disruption in male mice. Novartis Found Symp. 2005;268(4):78–89. source
  • Premisecitation

    In mice, exogenous testosterone was recently shown to increase social investigatory behaviour.

    “Also in mice, exogenous testosterone was recently shown to increase social investigatory behaviour [17].”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [17] Tejada LD, Rissman EF. Sex differences in social investigation: effects of androgen receptors, hormones and test partner. J Neuroendocrinol. 2012;24(8):1144–53. source
  • Premisecitation

    Ryan and co-workers showed that male C57BL/6J mice in the three-chambered apparatus test displayed equal amount of interest in the stimulus animal independent of its sex.

    “Ryan and co-workers showed that male C57BL/6J mice in the three-chambered apparatus test displayed equal amount of interest in the stimulus animal independent of its sex [27].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [27] Ryan BC, Young NB, Moy SS, Crawley JN. Olfactory cues are sufficient to elicit social approach behaviors but not social transmission of food preference in C57BL/6 J mice. Behav Brain Res. 2008;193(2):235–42. source
  • Findingown data

    In the first session, intact males spent significantly more time exploring stimulus animals than both female groups and GDX males.

    “In the first session of the social discrimination test, intact males spent a significantly greater amount of time exploring stimulus animals compared to both female groups and GDX males (between-group comparison p < 0.001; Fig. 3a).”
    Quote in the paperSubstantial claim
  • Findingown data

    In the first session, males spent equal time investigating GDX and intact stimulus animals.

    “In the first session of the social discrimination test, where focal mice investigated one novel mouse caged in a wire corral, males spent equal time investigating the GDX animal compared to the time investigating the intact stimulus animal (Fig. 2a).”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. 31
  • May combine two claims. 15

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Estrogens improve social recognition in mice through estrogen receptors.

    “estrogens are known to improve social recognition in mice through estrogen receptors [18, 19]”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [18] Choleris E, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW, Ogawa S. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proc Natl Acad Sci USA. 2003;100(10):6192–7. source
    • cites [19] Tang AC, Nakazawa M, Romeo RD, Reeb BC, Sisti H, McEwen BS. Effects of long-term estrogen replacement on social investigation and social memory in ovariectomized C57BL/6 mice. Horm Behav. 2005;47(3):350–7. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Testosterone treatment modulated neural responses to emotional faces.

    “modulated the neural responses to emotional faces [6]”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [6] Bos PA, van Honk J, Ramsey NF, Stein DJ, Hermans EJ. Testosterone administration in women increases amygdala responses to fearful and happy faces. Psychoneuroendocrinology. 2013;38(6):808–17. source

  • Classified as probably not a substantial claim.

    Premisecitation

    Variations in testosterone levels have been suggested to partially explain some of these differences.

    “variations in testosterone levels have been suggested to partially explain some of these differences [4]”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [4] Baron-Cohen S, Lombardo MV, Auyeung B, Ashwin E, Chakrabarti B, Knickmeyer R. Why are autism spectrum conditions more prevalent in males? PLoS Biol. 2011;9(6):e1001081. source

  • Classified as probably not a substantial claim.

    Premisecitation

    Some studies have shown sex differences in the duration of social investigation.

    “Some studies have shown sex differences in the duration of social investigation [12–14]”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites [12] Johnston AL, File SE. Sex differences in animal tests of anxiety. Physiol Behav. 1991;49(2):245–50. source
    • cites [13] Holmes MM, Niel L, Anyan JJ, Griffith AT, Monks DA, Forger NG. Effects of Bax gene deletion on social behaviors and neural response to olfactory cues in mice. Eur J Neurosci. 2011;34(9):1492–9. source
    • cites [14] Dumais KM, Bredewold R, Mayer TE, Veenema AH. Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region- and sex- specific ways. Horm Behav. 2013;64(4):693–701. source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Testosterone treatment decreased trust and cognitive empathy.

    “testosterone treatment decreased trust and cognitive empathy [5]”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [5] Bos PA, Terburg D, van Honk J. Testosterone decreases trust in socially naive humans. Proc Natl Acad Sci USA. 2010;107(22):9991–5. source

      The Results report that testosterone reduced interpersonal trust, particularly among participants with high baseline trust. The paper does not report a cognitive-empathy outcome; its reference to a separate facial-mimicry study concerns empathetic behavior, not cognitive empathy. (LLM, conf=0.89)

      Experimental — accuracy not yet measured

  • Classified as probably not a substantial claim.

    Premisecitation

    Testosterone has been suggested to be involved in sex differences in the duration of social investigation.

    “testosterone has been suggested to be involved [15–17]”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites [15] Thor DH, Wainwright KL, Holloway WR. Persistence of attention to a novel conspecific: some developmental variables in laboratory rats. Dev Psychobiol. 1982;15(1):1–8. source
    • cites [16] Thor DH. Testosterone and persistance of social investigation in laboratory rats. J Comp Physiol Psychol. 1980;94(5):970–6. source
    • cites [17] Tejada LD, Rissman EF. Sex differences in social investigation: effects of androgen receptors, hormones and test partner. J Neuroendocrinol. 2012;24(8):1144–53. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Estrogen receptor-alpha, and to some extent estrogen receptor-beta, are crucial for social memory in females.

    “A number of investigations have shown that estrogen receptor-alpha, and to some extent estrogen receptor-beta, are crucial for social memory in females [18, 29, 30].”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [18] Choleris E, Gustafsson JA, Korach KS, Muglia LJ, Pfaff DW, Ogawa S. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-alpha and -beta knockout mice. Proc Natl Acad Sci USA. 2003;100(10):6192–7. source
    • cites [29] Sanchez-Andrade G, Kendrick KM. Roles of alpha- and beta-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Horm Behav. 2011;59(1):114–22. source
    • cites [30] Morgan MA, Pfaff DW. Estrogen’s effects on activity, anxiety, and fear in two mouse strains. Behav Brain Res. 2002;132(1):85–93. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In a recent study, elevated social investigation was seen in males when comparing estrogen-treated males and females, exploring either GDX female or male conspecifics.

    “In a recent study, elevated social investigation was seen in males when comparing estrogen-treated males and females, exploring either GDX female or male conspecifics.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [17] Tejada LD, Rissman EF. Sex differences in social investigation: effects of androgen receptors, hormones and test partner. J Neuroendocrinol. 2012;24(8):1144–53. source

      The Results sections on female and male conspecifics report greater investigation by E2-treated WT males than WT females. However, Materials and methods > Stimulus animals specifies that the female stimuli were ovariectomised while the male stimuli were gonad-intact; it does not support describing both as GDX. Page numbers were not available in our copy. (LLM, conf=0.88)

      Experimental — accuracy not yet measured

  • Classified as probably not a substantial claim.

    Premisecitation

    More brain areas are activated during the encoding phase in men than in women.

    “In addition, it has been shown that more brain areas are activated during the encoding phase in men than in women [40, 41].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [40] Ino T, Nakai R, Azuma T, Kimura T, Fukuyama H. Gender differences in brain activation during encoding and recognition of male and female faces. Brain Imaging Behav. 2010;4(1):55–67. source
    • cites [41] Prince SE, Dennis NA, Cabeza R. Encoding and retrieving faces and places: distinguishing process- and stimulus-specific differences in brain activity. Neuropsychologia. 2009;47(11):2282–9. source

      The Methods > Subjects section reports the participants’ sex, but the Methods > fMRI analyses section describes comparisons by stimulus, encoding versus retrieval, and memory success—not by sex. Searches for men versus women and gender differences found no passage comparing the number of brain areas activated during encoding. (LLM, conf=0.76)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In that recent study, no sex differences were seen when all test animals were treated with testosterone, possibly due to an increased sociability in the female group.

    “No sex differences were however seen when all test animals were treated with testosterone—possibly due to an increased sociability in the female group [17].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [17] Tejada LD, Rissman EF. Sex differences in social investigation: effects of androgen receptors, hormones and test partner. J Neuroendocrinol. 2012;24(8):1144–53. source

  • May combine two claims.

    Findingown data

    Average plasma testosterone levels were 6.1 ± 0.6 ng/ml for males, 0.1 ± 0.1 for females, 0.1 ± 0.1 for GDX females, and 0.07 ± 0.3 for GDX males.

    “In the animals used for experiments the male group had an average testosterone level of 6.1 ± 0.6 ng/ml, females 0.1 ± 0.1 ng/ml, GDX females 0.1 ± 0.1 ng/ml and GDX males 0.07 ± 0.3 ng/ml.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    Intact females showed elevated basal locomotor activity.

    “the intact females showed elevated basal locomotor activity”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Social recognition ability is intact in intact males, gonadectomised males, and intact females.

    “the ability to recognise other individuals is intact in males with and without gonads, as well as in intact females”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Intact and GDX males, as well as intact females, display social recognition in the social discrimination paradigm.

    “The results from the social discrimination paradigm propose that intact and GDX males, as well as intact females, display social recognition.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In the first session of the novel object recognition test, all four groups spent equal amounts of time investigating the two similar objects, showing no preference for side or other factors.

    “In the first session of the novel object recognition test, where mice investigated two similar objects, all four groups spent equal amount of time investigating the two novel objects showing no preference for side, or other factors (between-group comparison p = 0.2; Fig. 5a).”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Women perform better than men in tasks measuring emotion recognition.

    “women perform better than men in tasks measuring face memory [1] and emotion recognition [2]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [2] Thompson AE, Voyer D. Sex differences in the ability to recognise non-verbal displays of emotion: a meta-analysis. Cogn Emot. 2014;28(7):1164–95. source

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    The results seem to contrast what is known from human studies.

    “As these results seem to contrast what is known from human studies”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Data from three animals was lost due to computer problems, leaving 54 animals.

    “Data from three animals (two intact male and one GDX females) was lost, due to computer problems during testing, leaving a total of 54 animals.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Women gaze more at the eyes of others.

    “Women also gaze more at the eyes of others [3]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Hall C, Hogue T, Guo K. Differential gaze behavior towards sexually preferred and non-preferred human figures. J Sex Res. 2011;48(5):461–9. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Women perform better than men in tasks measuring face memory.

    “women perform better than men in tasks measuring face memory [1]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Herlitz A, Reuterskiold L, Loven J, Thilers PP, Rehnman J. Cognitive sex differences are not magnified as a function of age, sex hormones, or puberty development during early adolescence. Dev Neuropsychol. 2013;38(3):167–79. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    One intact female was considered as an outlier and excluded from the study.

    “One intact female was considered as an outlier (>±2 SD from mean) and was excluded from the study.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Sex differences in social preference and social memory are rather established in humans.

    “sex differences in social preference and social memory are rather established in humans”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Two mice did not survive the surgery procedure.

    “In total, two mice did not survive the surgery procedure.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Testosterone treatment modulated neural responses to crying infants in women.

    “to crying infants in women [7]”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Bos PA, Hermans EJ, Montoya ER, Ramsey NF, van Honk J. Testosterone administration modulates neural responses to crying infants in young females. Psychoneuroendocrinology. 2010;35(1):114–21. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Some studies have shown effects of testosterone on long-term social recognition in rats.

    “some studies have shown effects of testosterone on long-term social recognition in rats [20, 21]”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [20] Bluthe RM, Schoenen J, Dantzer R. Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res. 1990;519(1–2):150–7. source
    • cites [21] Bluthe RM, Gheusi G, Dantzer R. Gonadal steroids influence the involvement of arginine vasopressin in social recognition in mice. Psychoneuroendocrinology. 1993;18(4):323–35. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Scoring was performed by one trained observer unaware of the status of the mice.

    “Scoring these behaviours was performed by one trained observer, who was unaware of the status of the mice.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    These results seem to contrast with what is seen in humans.

    “As these results seem to contrast with what is seen in humans”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Testosterone elevates social investigatory behaviour in females by acting on androgen receptors and not on estrogen receptors after conversion to estradiol.

    “This indicates that testosterone elevates social investigatory behaviour in females by acting on androgen receptors and not on estrogen receptors after conversion to estradiol.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Early studies suggested that female and castrated male rats hold social memories for longer time than intact males.

    “Additionally, early studies suggested that female and castrated male rats hold social memories for longer time than intact males [21, 31].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [21] Bluthe RM, Gheusi G, Dantzer R. Gonadal steroids influence the involvement of arginine vasopressin in social recognition in mice. Psychoneuroendocrinology. 1993;18(4):323–35. source
    • cites [31] Bluthe RM, Dantzer R. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res. 1990;535(2):301–4. source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Previous studies have shown that only intact and GDX male rats substituted with testosterone display object memory, in contrast to GDX males treated with oil or estradiol.

    “Previous studies have shown that only intact and GDX male rats substituted with testosterone display object memory, in contrast to GDX males treated with oil or estradiol [32].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [32] Aubele T, Kaufman R, Montalmant F, Kritzer MF. Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. Horm Behav. 2008;54(2):244–52. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Ceccarelli et al. reported that male rats show more persistence investigating the objects compared to female rats.

    “In line with our results, Ceccarelli et al. [33], reported that male rats show more persistence investigating the objects compared to female rats.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [33] Ceccarelli I, Scaramuzzino A, Aloisi AM. Effects of gonadal hormones and persistent pain on non-spatial working memory in male and female rats. Behav Brain Res. 2001;123(1):65–76. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    The differences in results between our study and previous studies may be explained by our considerably shorter inter-trial delay (30 vs. 90 min).

    “The differences in results may be explained by our considerably shorter inter-trial delay (30 vs. 90 min).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationcitation

    Strict comparisons of our results with the other studies are problematic because of several differences in study designs, type of paradigms, and steroid treatment regimes.

    “Since there are several differences between their study and ours with respect to study designs, type of paradigms and steroid treatment regimes in the other studies, strict comparisons of our results are problematic [17].”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data

    This study did not include information about estrus cycle phase, so it could not confirm the previously reported importance of estrus cycle phase for social recognition.

    “Since this study did not include information about estrus cycle phase we could not confirm its previously reported importance for social recognition [28, 29].”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation

    Studies in humans give reason to think that female mice may encode social information more efficiently than males, which could contribute to explaining our results.

    “However, studies in humans give us reason to think that also female mice may encode social information more efficiently than males, which could contribute to explaining our results.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductown data

    The current study did not test for long-term social recognition, so the effects of longer social memory cannot be seen.

    “These effects cannot be seen in the current study as we did not test for long-term social recognition.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Intact male mice have higher social investigatory behaviour compared to intact females, GDX males, and GDX females.

    “Our results clearly show that intact male mice have higher social investigatory behaviour compared to intact females, as well as GDX males and females.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Based on these findings, it was suggested that women more efficiently recruit relevant brain regions for encoding memories.

    “Based on these findings it was suggested that women more efficiently recruit relevant brain regions for encoding memories.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Estrogen receptors influence long-term, but not short-term, social recognition in male mice.

    “In contrast, the estrogen receptors influence long-term, but not short-term, social recognition in male mice [29].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] Sanchez-Andrade G, Kendrick KM. Roles of alpha- and beta-estrogen receptors in mouse social recognition memory: effects of gender and the estrous cycle. Horm Behav. 2011;59(1):114–22. source

  • May combine two claims.

    Interpretationown data

    Previous findings support the results of our study showing that all groups have object recognition memory although females showed lower levels of general interest in novel objects.

    “Taken together, previous findings support the results of our study showing that all groups have object recognition memory although females showed lower levels of general interest in novel objects.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Previous human studies using the face recognition paradigm propose that women are better than men at encoding information, rather than having better face recognition memory as such.

    “Previous human studies using the face recognition paradigm, propose that women are better than men at encoding information, rather than having better face recognition memory as such [39].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [39] Weirich S, Hoffmann F, Meissner L, Heinz A, Bengner T. Sex influence on face recognition memory moderated by presentation duration and reencoding. Neuropsychology. 2011;25(6):806–13. source
41 of 41

  • The paper relies on this without support.

    Testosterone is crucial for sexual dimorphisms in social behaviours in rodents and other vertebrates.

    “In rodents and other vertebrates, it is well-established that testosterone is crucial for sexual dimorphisms in social behaviours, such as aggression, mating behaviours and parental behaviours.”

  • The paper relies on this without support.

    The risk for autism spectrum disorders is lower in girls than in boys.

    “the risk for autism spectrum disorders is lower in girls than in boys”

  • The paper relies on this without support.

    The underlying causative factors for sex differences in social preference and social memory in humans are unknown.

    “the underlying causative factors for these differences are unknown”

  • The paper relies on this without support.

    The importance of sex and gonadal hormones has not been evaluated in the three-chambered apparatus test measuring sociability and social investigation.

    “The importance for sex and gonadal hormones has, so far, not been evaluated in the three-chambered apparatus test measuring sociability and social investigation.”

  • The paper relies on this without support.

    The three-chambered apparatus test is often used when aiming to understand social deficits seen in autism spectrum disorders.

    “the three-chambered apparatus test is often used when aiming to understand social deficits seen in autism spectrum disorders”

  • The paper relies on this without support.

    Autism spectrum disorders have higher prevalence in males.

    “a group of disorders with higher prevalence in males”

  • The paper relies on this without support.

    It is not clarified to what extent testis hormones modulate social discrimination in male mice.

    “it is not clarified to what extent testis hormones modulate social discrimination in male mice”

  • The paper relies on this without support.

    It is not clarified if social recognition is sexually dimorphic in mice.

    “and if social recognition is sexually dimorphic in mice”

  • The paper relies on this without support.

    There are inconsistencies and gaps in the knowledge about the role of sex and testosterone for social recognition and social preference.

    “there are inconsistencies and gaps in the knowledge about the role of sex and testosterone for social recognition and social preference”

  • The paper relies on this without support.

    Olfactory cues are crucial for social behaviours in mice.

    “Since olfactory cues are crucial for social behaviours in mice”
10 of 10

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conflicting sampling duration for validation experiments A and B

    Minor

    The methods state that experiments A and B used a 5-minute sampling session, but the Fig. 1 caption describes their sampling session as 10 minutes.

1 of 1

Cites

Flagged first, then by citations

Cited by

Sorted by citations

Related

Authors
Karlsson, S. A., Haziri, K., Hansson, E., Kettunen, P., & Westberg, L.
Affiliations
University of Gothenburg (SE)
Corresponding author
Karlsson, Sara A.
ORCID
Venue
BMC Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2015-11-25
Volume
16
Issue
1
Pages
83-83
ISSN
1471-2202 (ISSN-L)
DOI
10.1186/s12868-015-0221-z
PMC
PMC4660658
OpenAlex
W2175793031
Semantic Scholar
699674ca3450382e7cbd41e78ded1954a1e5369e
Cited by
72
References
45
Citations by year
2026: 7 · 2025: 2 · 2024: 10 · 2023: 10 · 2022: 10 · 2021: 6 · 2020: 7 · 2019: 8 · 2018: 7 · 2017: 3 · 2016: 2
FWCI
6.27
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • BMC Neuroscience (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (submittedVersion, cc-by)
  • PubMed Central (submittedVersion, cc-by)
Funders
  • Vetenskapsrådet (SE) (2009-7006; 2011-4819)
  • Märtha Lundqvists stiftelse (N/A)
  • NovoNordisk Foundation
  • Fredrik och Ingrid Thurings Stiftelse (SE)
  • Magnus Bergvalls Stiftelse (SE)
  • Ake Wibergs Stiftelse (SE)
  • Åhlén-stiftelsen (SE)
  • Jeanssons-stiftelsen
  • Stiftelsen Söderström-Königska sjukhemmet
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Keywords
sex differences, gonadectomy, social investigation, social recognition, sociability, gonadal hormones, testicular hormones, social discrimination, object recognition, locomotor activity, animal models of autism, mice
MeSH terms
Animals, Discrimination, Psychological, Female, Habituation, Psychophysiologic, Male, Mice, Inbred C57BL, Orchiectomy, Ovariectomy, Psychological Tests, Sex Characteristics, Social Behavior, Recognition, Psychology, Models, Animal, Gonadal Hormones, Olfactory Perception

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-12.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-12.

Cited sources are checked by gpt-6-sol.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review