Excess Neonatal Testosterone Causes Male-Specific Social and Fear Memory Deficits in Wild-Type Mice
Open accessPublished version of a preprint
Abstract
Neurodevelopmental disorders disproportionately affect males compared with females. The biological mechanisms of this male susceptibility or female protection have not been identified. There is evidence that fetal/neonatal gonadal hormones, which play a pivotal role in many aspects of development, may contribute. Here, we investigate the effects of excess testosterone (T) during a critical period of sex-specific brain organization on social approach and fear learning behaviors in C57BL/6J wild-type mice. Male, but not female, mice treated with T on the day of birth (Postnatal Day 0; PN0) exhibited decreased social approach as juveniles and decreased contextual fear memory as adults, compared with vehicle (veh)-treated controls. These deficits were not driven by anxiety-like behavior or changes in locomotion or body weight. Mice treated with the same dose of T on PN18, which is outside of the critical period of brain masculinization, did not demonstrate impairments compared with the veh group. These findings indicate that excess T during a critical period of early development, but not shortly after, induces long-term deficits relevant to the male sex bias in neurodevelopmental disorders.
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Written from the paper’s full text.
TL;DR
A single neonatal testosterone propionate injection (100 μg) on postnatal day 0, but not postnatal day 18, caused male-specific decreases in juvenile social approach and adult contextual fear memory in C57BL/6J wild-type mice, with no effects in females. These behavioral deficits were not explained by body weight, locomotion, or anxiety-like behavior.
Key findings
- PN0 testosterone-treated males had a lower social preference index in the choice phase than Males+Veh, Females+Veh, and Females+T (p=0.013, 0.039, and 0.038, respectively); two-way ANOVA showed a main effect of treatment (F(1,65)=5.743, p=0.019, η2=0.073) and a sex × treatment trend (F(1,65)=3.827, p=0.055).
- PN0 testosterone-treated males showed lower 24-h contextual fear freezing than Males+Veh, Females+Veh, and Females+T (p=0.029, 0.034, and 0.035, respectively); two-way ANOVA showed main effects of sex (F(1,40)=4.514, p=0.040), treatment (F(1,40)=4.310, p=0.044), and interaction (F(1,40)=4.269, p=0.045).
- The deficits were not driven by anxiety-like behavior, locomotion, or body weight: elevated zero maze distance and open-arm time showed no significant effects, social approach distance traveled showed no significant effects, and no significant testosterone-driven weight differences within sexes were found at any age.
- The same testosterone dose on PN18 did not impair social approach or contextual fear memory; for example, choice-phase preference index showed no treatment effect (F(1,39)=0.001, p=0.971), and 24-h fear freezing showed no treatment effect (F(1,47)=0.605, p=0.441).
Methods
- C57BL/6J mice were used; litters were randomly assigned to testosterone propionate (100 μg in 20 μl sesame oil) or vehicle (20 μl sesame oil) subcutaneously on PN0 or PN18. A total of 205 mice were used for behavioral testing, with 21 excluded; gonadectomized A/J mice served as social stimuli.
- Social approach was tested at PN28–32 in a three-chamber arena with 10-min habituation and choice phases and a preference index; contextual fear conditioning was tested at PN53–64 with a single 1.5 mA, 2-s footshock and a 24-h memory test. Separate cohorts were used for weight measurement and elevated zero maze.
- Analyses used GraphPad Prism 9: two-way ANOVA with sex and treatment as main effects plus sex × treatment interaction, Tukey post hoc tests, repeated-measures three-way ANOVA for weight, p<0.05, and eta squared for effect sizes.
Limitations
- Stated: the study used a single moderate testosterone dose; entire litters received the same treatment and same-treatment mice were housed together; mechanisms were not identified; human translation is limited by ethical constraints and unknown relationships between blood/brain testosterone and accessible samples; the manipulation is not presented as a model of any specific disorder.
- Evident: no direct measurements of testosterone levels, receptor pathways, or brain circuits are reported; only one mouse strain and two treatment time points were tested; some PN0 mice underwent social testing before fear conditioning, so testing-order effects are not ruled out.
Model-written summary. Check it against the paper before relying on it.
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Cites
Statistics
Claims the paper makes
10 of 25 cited sources checked · 4 supported · 0 flagged · accuracy not yet measured
- Premisecitation
Males exposed to increased levels of steroidogenic factors in amniotic fluid are more likely to be diagnosed with ASD.
“There is evidence that males exposed to increased levels of steroidogenic factors in amniotic fluid, likely indicating fetal origin, are more likely to be diagnosed with ASD (Baron-Cohen et al., 2015).”
Quote in the paperSubstantial claim1 of 1 sources checked- cites Baron-Cohen et al., 2015 source
- Study design and conductcitation
Vehicle-treated mice exhibited behavior statistically equivalent to historical never-injected control mice for social preference at ~PN30 and 24 hr fear memory at ~PN60.
“veh-treated mice exhibited behavior statistically equivalent to historical data of ours with mice that were undisturbed as neonates (no neonatal injection)”
- Also stated in: § Discussion · plain
“both social preference indices at ~PN30 and 24 hr fear memory results at ~PN60 were comparable between mice administered veh and never-injected control mice we have collected over various experiments”
Quote in the paperSubstantial claim3 of 3 sources checked- cites Ferri et al., 2021 source
The Results sections compare Pcdh10 mutant mice with wild-type littermates, not vehicle-treated mice with historical never-injected controls. The copy describes 24-hour fear tests, but the passages found do not report a statistical comparison involving neonatal injections or social preference; searches for those terms did not locate one. Page numbers were not available. (LLM, conf=0.75)
Experimental — accuracy not yet measured - cites Ferri et al., 2020 source
Materials and Methods (Behavior; page unavailable) describes social-approach testing at about 30 and 70 days, but not vehicle-treated or never-injected mice. The Discussion (page unavailable) compares 70-day sniffing with previously collected data from naïve mice; it does not report statistical equivalence after neonatal injections. Searches for vehicle treatment, neonatal injection, and 24-hour fear memory found no passage establishing the claimed comparison. (LLM, conf=0.76)
Experimental — accuracy not yet measured - cites Schoch et al., 2017 source
The Methods and Materials > Behavior section describes social-approach testing at 28–32 days and a separate cohort injected with saline or d-cycloserine 30 minutes before testing. Our copy does not report a statistical comparison with historical never-injected mice, neonatal vehicle injections, or 24-hour fear memory at approximately PN60 (searched those terms and their paraphrases). (LLM, conf=0.77)
Experimental — accuracy not yet measured
- Also stated in: § Discussion · plain
- Findingown data
Neonatal testosterone treatment on PN0 did not affect body weight within sexes at any age.
“Mice that underwent treatment with neonatal testosterone had similar body weight to those treated with veh on the day of birth (Fig. 4A).”
- Also stated in: § Social and fear memory deficits are not due to differences in body weight or anxiety-like behavior · plain
“there were no significant differences driven by testosterone within sexes at any age.”
Quote in the paperSubstantial claim - Also stated in: § Social and fear memory deficits are not due to differences in body weight or anxiety-like behavior · plain
- Findingown data
Neonatal testosterone treatment on PN0 did not affect distance traveled during the social approach test in juvenile mice.
“Neonatal testosterone treatment had no effects on distance traveled during the social approach test.”
- Also stated in: § A single testosterone treatment on the day of birth results in male-specific social approach deficits in juveniles · plain
“Therefore, the decrease in social approach in juvenile males treated neonatally with testosterone was not an effect of altered locomotor behavior.”
Quote in the paperSubstantial claim - Also stated in: § A single testosterone treatment on the day of birth results in male-specific social approach deficits in juveniles · plain
- Findingown data
Treatment with the same dose of testosterone on PN18 did not affect social approach in juvenile mice compared to vehicle.
“During the choice phase of the social approach test, all groups had a similar PI; a two-way ANOVA produced no main effects of sex (F(1,39)=0.084, p=0.773, η2=0.022) or treatment (F(1,39)=0.001, p=0.971, η2=0.00003), and no interaction of the two (F(1,39)=0.120, p=0.731, η2=0.003; Fig. 5B).”
- Also stated in: § Abstract · boosted
“Mice treated with the same dose of testosterone on postnatal day 18 (PN18), which is outside of the critical period of brain masculinization, did not demonstrate impairments compared to the vehicle group.”
Quote in the paperSubstantial claim - Also stated in: § Abstract · boosted
- Findingown data
Treatment with the same dose of testosterone on PN18 did not affect contextual fear memory in adult mice compared to vehicle.
“Twenty-four hours later, freezing percentages were similar across all groups. A two-way ANOVA showed no significant main effect of sex (F(1,47)=2.513, p=0.120, η2=0.049) or treatment (F(1,47)=0.605, p=0.441, η2=0.012), and no interaction (F(1,47)=1.421, p=0.239, η2=0.028; Fig. 6B).”
Quote in the paperSubstantial claim - Findingown data
Neonatal testosterone treatment on PN0 did not affect anxiety-like behavior or locomotion in adult mice as measured by the elevated zero maze.
“Naïve adult mice treated on the day of birth with testosterone did not show any differences in distance traveled or percent time spent in open arms in the elevated zero maze compared to those treated with vehicle on the day of birth (Fig 4B and 4C).”
Quote in the paperSubstantial claim - Findingnone given
The observed social and fear memory deficits in testosterone-treated mice were not due to changes in body weight or motor activity.
“Importantly, the observed deficits were not due to changes in body weight or motor activity that may affect general function or indicate global disruptions in physical development.”
Quote in the paperSubstantial claim - Findingcitation
The observed deficits were not attributed to heightened anxiety-like behavior.
“The deficits were also not attributed to heightened anxiety-like behavior, which can co-occur with social deficits (Allsop et al., 2014; Felix-Ortiz et al., 2016).”
Quote in the paperSubstantial claim - Interpretationown data
The social and fear memory deficits in PN0 testosterone-treated males were not driven by changes in anxiety-like behavior, locomotion, or body weight.
“These deficits were not driven by anxiety-like behavior or changes in locomotion or body weight.”
Quote in the paperSubstantial claim - Premisecitation
In rodents, many important and irreversible sex hormone-mediated effects on brain development are complete by postnatal day 10.
“In rodents, many important and irreversible sex hormone-mediated effects on brain development are complete by postnatal day 10 (Davis et al., 1996; McCarthy et al., 2017).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Davis et al., 1996 source
- cites McCarthy et al., 2017
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Amniotic testosterone level is correlated with ASD-related traits in children regardless of diagnosis.
“Amniotic testosterone level is correlated with ASD-related traits in children regardless of diagnosis (Auyeung et al., 2012, 2010; Chapman et al., 2006; Knickmeyer and Baron-Cohen, 2006; Lutchmaya et al., 2002a, 2002b).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
Excess testosterone during a critical period of early development, but not shortly after, induces long-term deficits relevant to the male sex bias in neurodevelopmental disorders.
“These findings indicate that excess testosterone during a critical period of early development, but not shortly after, induces long-term deficits relevant to the male sex bias in neurodevelopmental disorders.”
Quote in the paperSubstantial claim - Interpretationown data
Excess testosterone in early development alone is sufficient to induce neurodevelopmental deficits in mice.
“However, we have shown that excess testosterone in early development alone is sufficient to induce neurodevelopmental deficits in mice, which paves the way for future studies.”
Quote in the paperSubstantial claim - Premisecitation
In rodents, postnatal day 18 is outside the critical period of sex-specific brain masculinization.
“Mice treated with the same dose of testosterone on postnatal day 18 (PN18), which is outside of the critical period of brain masculinization, did not demonstrate impairments compared to the vehicle group.”
- Also stated in: § Discussion · plain
“postnatal day 18 was chosen as a timepoint outside the endogenous testosterone activity (Davis et al., 1996; McCarthy et al., 2017).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Davis et al., 1996 source
- cites McCarthy et al., 2017
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Also stated in: § Discussion · plain
- Premisecitation
The single moderate dose and timing of testosterone used in this study has been shown to masculinize a female rodent brain.
“This dose and timing was chosen because it has been shown to masculinize a female rodent brain”
Quote in the paperSubstantial claim0 of 3 sources checked
- Classified as probably not a substantial claim. 10
- May combine two claims. 8
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAutism Spectrum Disorder (ASD) affects males at approximately a 4 to 1 ratio compared to females.
“For example, Autism Spectrum Disorder (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) affect males at a ~4 and ~2 to 1 ratio, respectively (Maenner et al., 2023; Yang et al., 2022).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Maenner et al., 2023 source
May combine two claims.
PremisecitationHuman male testosterone production surges mid-gestation and shortly after birth, while male rodents have highest levels several days before and after birth; females of those species are exposed to significantly lower levels of gonadal hormones during early development.
“Human male testosterone production surges mid-gestation and shortly after birth, while male rodents have highest levels several days before and after birth. Females of those species are exposed to significantly lower levels of gonadal hormones during early development (Gillies and McArthur, 2010a; McCarthy, 2011).”
Quote in the paperSubstantial claim1 of 2 sources checked- cites Gillies and McArthur, 2010a
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites McCarthy, 2011 source
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Classified as probably not a substantial claim. May combine two claims.
PremisecitationMany social behaviors exhibit sex differences and are sensitive to gonadal hormones and endocrine disruptors.
“Many social behaviors exhibit sex differences and are sensitive to gonadal hormones and endocrine disruptors (Bell, 2018).”
Quote in the paperSubstantial claim1 of 1 sources checked- cites Bell, 2018 source
Classified as probably not a substantial claim.
PremisecitationA single dose of testosterone propionate (100 μg) has been shown to masculinize a female rodent brain.
“Testosterone propionate (Sigma; 100μg in 20 μl sesame oil, a dose previously shown to induce brain masculinization in a female rodent) (Ghahramani et al., 2014; Goel and Bale, 2013; Hisasue et al., 2010; Nakachi et al., 2015; Seney et al., 2012)”
Quote in the paperSubstantial claim1 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAcquisition of conditioned fear and fear extinction is impaired in psychopathy, PTSD, anxiety, and other disorders.
“Acquisition of conditioned fear and fear extinction is impaired in psychopathy, PTSD, anxiety, and other, disorders (VanElzakker et al., 2014; Veit et al., 2013).”
Quote in the paperNot a substantial claim2 of 2 sources checked- cites VanElzakker et al., 2014 source
Section 5.1.2 reports abnormal fear responses during acquisition and impaired extinction in PTSD; Section 6.1 reports resistance to extinction in other anxiety disorders. The source does not establish impaired acquisition across those anxiety disorders—it reports normal acquisition in one panic-disorder study—and the passages do not address psychopathy. Page numbers are unavailable in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured - cites Veit et al., 2013 source
The Results and Discussion report deficient acquisition of conditioned fear responses in highly psychopathic offenders, particularly those scoring high on the affective facet. Although the Experimental design includes an extinction phase, the paper does not establish impaired fear extinction. It does not study PTSD, anxiety, or other disorders; those parts of the jointly cited sentence are not supported by Veit et al. (LLM, conf=0.87)
Experimental — accuracy not yet measured
May combine two claims.
Findingown dataIn C57BL/6J wild-type mice, treatment with testosterone on the day of birth (PN0) decreased social approach in juvenile males compared to vehicle-treated controls, but not in females.
“Male, but not female, mice treated with testosterone on the day of birth (PN0) exhibited decreased social approach as juveniles and decreased contextual fear memory as adults, compared to vehicle-treated controls.”
- Also stated in: § A single testosterone treatment on the day of birth results in male-specific social approach deficits in juveniles · plain
“A Tukey post hoc test indicated that males treated on PN0 with testosterone (Males + T) had significantly lower PI than Males + Veh, Females + Veh, and Females + T (p=0.013, 0.039, and 0.038, respectively; Fig. 2B).”
Quote in the paperSubstantial claim- Also stated in: § A single testosterone treatment on the day of birth results in male-specific social approach deficits in juveniles · plain
May combine two claims.
Findingown dataIn C57BL/6J wild-type mice, treatment with testosterone on PN0 decreased contextual fear memory in adult males compared to vehicle-treated controls, but not in females.
“Male, but not female, mice treated with testosterone on the day of birth (PN0) exhibited decreased social approach as juveniles and decreased contextual fear memory as adults, compared to vehicle-treated controls.”
- Also stated in: § A single testosterone treatment on the day of birth results in male-specific contextual fear conditioning deficits in adults · plain
“A Tukey post hoc test indicated that males treated on PN0 with testosterone (Males + T) had significantly lower freezing than Males + Veh, Females + Veh, and Females + T (p=0.029, 0.034, and 0.035, respectively; Fig. 3B).”
Quote in the paperSubstantial claim- Also stated in: § A single testosterone treatment on the day of birth results in male-specific contextual fear conditioning deficits in adults · plain
May combine two claims.
Findingown dataNeonatal testosterone treatment did not affect mortality, with comparable litter sizes between vehicle and testosterone groups (veh 6.735 ± 0.392 vs T 5.970 ± 0.388, p=0.1700).
“Notably, neonatal testosterone treatment did not affect mortality; litter size was 6.735 ± 0.392 for veh and 5.970 ± 0.388 for T, p=0.1700.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAttention Deficit Hyperactivity Disorder (ADHD) affects males at approximately a 2 to 1 ratio compared to females.
“For example, Autism Spectrum Disorder (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) affect males at a ~4 and ~2 to 1 ratio, respectively (Maenner et al., 2023; Yang et al., 2022).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Yang et al., 2022 source
Checked before — its earlier verdict is held back until a new check runs.
May combine two claims.
Interpretationown dataThere is a sensitive period in which excess testosterone can disrupt sex-specific neural circuits and even a brief dysregulation of testosterone levels can induce long-lasting effects.
“Therefore, our results indicate that excess testosterone during development is not universally detrimental but there is a sensitive period in which excess testosterone can disrupt sex-specific neural circuits and even a brief dysregulation of testosterone levels can induce long-lasting effects.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataBoth social approach behavior and fear memory exhibit sex differences in vulnerability in early development.
“Additionally, these findings indicate that both social approach behavior and fear memory exhibit sex differences in vulnerability in early development, which has significant implications for neurodevelopmental and neuropsychiatric disorders that affect males and females differently in terms of prevalence, presentation, or progression.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationMaternal testosterone in the second trimester is associated with increased autism-relevant behaviors in male children.
“Maternal testosterone in the second trimester is associated with increased autism-relevant behaviors in male children (Firestein et al., 2022).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Firestein et al., 2022 source
Classified as probably not a substantial claim.
Study design and conductnone givenLitters were randomly divided into two experimental conditions: treatment with testosterone or vehicle.
“Litters were randomly divided into two experimental conditions: treatment with testosterone (T) or vehicle (veh; see below), receiving treatment on the day of birth (PN0) or on postnatal day 18 (PN18).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataA total of 205 mice were used for behavioral testing.
“A total of 205 mice were used for behavioral testing. Of the 205 mice, 21 were excluded due to inactivity during the testing period, excessive climbing on cylinders, or statistical outliers (>2SD from the mean).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenExperiments were conducted in accordance with IACUC policies and approved protocols, and according to ARRIVE guidelines.
“Experiments were conducted in accordance with the [Author University] Institutional Animal Care and Use Committee (IACUC) policies and approved protocols, and according to ARRIVE guidelines.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataOf the 205 mice, 21 were excluded due to inactivity during the testing period, excessive climbing on cylinders, or statistical outliers (>2SD from the mean).
“A total of 205 mice were used for behavioral testing. Of the 205 mice, 21 were excluded due to inactivity during the testing period, excessive climbing on cylinders, or statistical outliers (>2SD from the mean).”
Quote in the paperNot a substantial claim
The paper relies on this without support.
The mechanisms underlying sex differences in neurodevelopmental disorders are not fully understood.
“The mechanisms underlying these sex differences are not fully understood, but elucidating them would significantly improve risk assessment, early intervention, and targeted treatments.”
The paper relies on this without support.
Hormonal dysregulation during the critical period may cause sex-specific vulnerabilities to neurodevelopmental deficits.
“It is during the critical period that hormonal dysregulation may cause sex-specific vulnerabilities to neurodevelopmental deficits.”
The paper relies on this without support.
The effects of this dose and timing of testosterone on the male brain and behavior have not been described.
“the effects on the male brain and behavior have not been described”
Statistics that don’t add up
Each reported p-value recomputed from its test statistic and degrees of freedom.
Inconsistent p-value across alpha = .05: F(1,39)=0.105, p = .019
MajorThe paper reports p = .019 here; recomputing from the test statistic and its degrees of freedom gives p = .748. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p = .019 · recomputed p = .748
“F(1,39)=0.105, p=0.019”
Inconsistent p-value across alpha = .05: F(1,65)=8.17, p = .370
MajorThe paper reports p = .37 here; recomputing from the test statistic and its degrees of freedom gives p = .006. The two fall on opposite sides of alpha = .05. The check cannot tell whether the statistic or the p-value is the misprint.
Reported p = .37 · recomputed p = .006
“F(1,65)=8.17, p=0.370”
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Doesn’t add upF(1, 65) = 8.17reported p = .37 · recomputed p = .006The two fall on opposite sides of .05
“F(1,65)=8.17, p = .370”
- Doesn’t add upF(1, 39) = 0.105reported p = .019 · recomputed p = .748The two fall on opposite sides of .05
“F(1,39)=0.105, p = .019”
- Not confirmedF(1, 34) = 3.117reported p = .087 · recomputed p = .086
“F(1,34)=3.117, p = .087”
- Not confirmedF(1, 34) = 2.09reported p = .158 · recomputed p = .157
“F(1,34)=2.090, p = .158”
- ConsistentF(1, 65) = 0.2reported p = .656 · recomputed p = .656
“F(1,65)=0.200, p = .656”
- ConsistentF(1, 65) = 0.034reported p = .855 · recomputed p = .854
“F(1,65)=0.034, p = .855”
- ConsistentF(1, 65) = 2.188reported p = .144 · recomputed p = .144
“F(1,65)=2.188, p = .144”
- ConsistentF(1, 65) = 5.743reported p = .019 · recomputed p = .019
“F(1,65)=5.743, p = .019”
- ConsistentF(1, 65) = 3.827reported p = .055 · recomputed p = .055
“F(1,65)=3.827, p = .055”
- ConsistentF(1, 65) = 0.355reported p = .553 · recomputed p = .553
“F(1,65)=0.355, p = .553”
- ConsistentF(1, 65) = 2.008reported p = .161 · recomputed p = .161
“F(1,65)=2.008, p = .161”
- ConsistentF(1, 65) = 2.655reported p = .108 · recomputed p = .108
“F(1,65)=2.655, p = .108”
- ConsistentF(1, 65) = 1.029reported p = .314 · recomputed p = .314
“F(1,65)=1.029, p = .314”
- ConsistentF(1, 65) = 0.823reported p = .368 · recomputed p = .368
“F(1,65)=0.823, p = .368”
- ConsistentF(1, 65) = 0.697reported p = .407 · recomputed p = .407
“F(1,65)=0.697, p = .407”
- ConsistentF(1, 40) = 0.199reported p = .658 · recomputed p = .658
“F(1,40)=0.199, p = .658”
- ConsistentF(1, 40) = 2.067reported p = .158 · recomputed p = .158
“F(1,40)=2.067, p = .158”
- ConsistentF(1, 40) = 1.372reported p = .248 · recomputed p = .248
“F(1,40)=1.372, p = .248”
- ConsistentF(1, 40) = 4.514reported p = .04 · recomputed p = .040
“F(1,40)=4.514, p = .040”
- ConsistentF(1, 40) = 4.31reported p = .044 · recomputed p = .044
“F(1,40)=4.310, p = .044”
- ConsistentF(1, 40) = 4.269reported p = .045 · recomputed p = .045
“F(1,40)=4.269, p = .045”
- ConsistentF(2, 60) = 2525reported p < .0001 · recomputed p < .001
“F(2,60)=2525, p < .0001”
- ConsistentF(1, 29) = 12.69reported p = .001 · recomputed p = .001
“F(1,29)=12.69, p = .001”
- ConsistentF(1, 29) = 7.345reported p = .011 · recomputed p = .011
“F(1,29)=7.345, p = .011”
- ConsistentF(8, 232) = 41.04reported p < .0001 · recomputed p < .001
“F(8,232)=41.04, p < .0001”
- ConsistentF(8, 232) = 4.967reported p < .0001 · recomputed p < .001
“F(8,232)=4.967, p < .0001”
- ConsistentF(8, 232) = 2.556reported p < .011 · recomputed p = .011
“F(8,232)=2.556, p < .011”
- ConsistentF(1, 29) = 0.027reported p = .871 · recomputed p = .871
“F(1,29)=0.027, p = .871”
- ConsistentF(1, 34) = 0.102reported p = .751 · recomputed p = .751
“F(1,34)=0.102, p = .751”
- ConsistentF(1, 34) = 0.012reported p = .913 · recomputed p = .913
“F(1,34)=0.012, p = .913”
- ConsistentF(1, 34) = 0.623reported p = .435 · recomputed p = .435
“F(1,34)=0.623, p = .435”
- ConsistentF(1, 34) = 0.551reported p = .463 · recomputed p = .463
“F(1,34)=0.551, p = .463”
- ConsistentF(1, 39) = 0.01reported p = .922 · recomputed p = .921
“F(1,39)=0.010, p = .922”
- ConsistentF(1, 39) = 1.28reported p = .265 · recomputed p = .265
“F(1,39)=1.280, p = .265”
- ConsistentF(1, 39) = 0.586reported p = .449 · recomputed p = .449
“F(1,39)=0.586, p = .449”
- ConsistentF(1, 39) = 0.084reported p = .773 · recomputed p = .773
“F(1,39)=0.084, p = .773”
- ConsistentF(1, 39) = 0.001reported p = .971 · recomputed p = .975
“F(1,39)=0.001, p = .971”
- ConsistentF(1, 39) = 0.12reported p = .731 · recomputed p = .731
“F(1,39)=0.120, p = .731”
- ConsistentF(1, 39) = 0.153reported p = .698 · recomputed p = .698
“F(1,39)=0.153, p = .698”
- ConsistentF(1, 39) = 0.089reported p = .767 · recomputed p = .767
“F(1,39)=0.089, p = .767”
- ConsistentF(1, 39) = 0.345reported p = .561 · recomputed p = .560
“F(1,39)=0.345, p = .561”
- ConsistentF(1, 39) = 8.207reported p = .007 · recomputed p = .007
“F(1,39)=8.207, p = .007”
- ConsistentF(1, 39) = 0.286reported p = .596 · recomputed p = .596
“F(1,39)=0.286, p = .596”
- ConsistentF(1, 47) = 3.887reported p = .055 · recomputed p = .055
“F(1,47)=3.887, p = .055”
- ConsistentF(1, 47) = 0.779reported p = .382 · recomputed p = .382
“F(1,47)=0.779, p = .382”
- ConsistentF(1, 47) = 0.081reported p = .778 · recomputed p = .777
“F(1,47)=0.081, p = .778”
- ConsistentF(1, 47) = 2.513reported p = .12 · recomputed p = .120
“F(1,47)=2.513, p = .120”
- ConsistentF(1, 47) = 0.605reported p = .441 · recomputed p = .441
“F(1,47)=0.605, p = .441”
- ConsistentF(1, 47) = 1.421reported p = .239 · recomputed p = .239
“F(1,47)=1.421, p = .239”
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.
Fear-baseline interaction names a factor absent from the stated analysis
MinorThe Methods specify a sex × treatment interaction for these two-way ANOVAs, whereas the fear-baseline result reports a phase × sex interaction.
“no significant phase × sex interaction (F(1,47)=0.081, p=0.778, η2=0.031; Fig. 6A)”
“For all other data, a two-way ANOVA was performed with sex and treatment as main effects, and a sex × treatment interaction was also tested.”
PN18 locomotion treatment effect is called nonsignificant despite p=0.019
MinorThe reported p-value is below the paper's stated significance threshold, but the result is described as showing no main effect of treatment.
“no main effect of treatment (F(1,39)=0.105, p=0.019, η2=0.002)”
“Significance was set to p<0.05.”
Conflicting counts of PN18 mice tested only for fear conditioning
MinorOne Methods passage says 7 of 51 PN18-treated mice underwent only fear conditioning; another says 8 additional mice did not undergo social testing.
“except for 7/51 mice underwent only fear conditioning as adults.”
“Of the mice treated at PN18, 44 were tested at PN28–32 for social approach and all were subsequently tested at PN53–64 for fear conditioning plus an additional 8 that did not undergo social testing due to a scheduling issue.”
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“…neuropeptide signaling, neurogenesis, synaptic programming, and cell differentiation, migration, and death are in fl uenced by gonadal hormones during development and may be involved in the social and fear memory de fi cits (Baron-Cohen et al., 2005, 2011; Schaafsma et al., 2017; Ferri et al., 2018).”
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Cerebellar modulation of the reward circuitry and social behavior
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Attention-deficit/hyperactivity disorder and social dysfunctioning
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Prefrontal Cortex and Social Cognition in Mouse and Man
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From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders
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“Acquisition of conditioned fear and fear extinction is impaired in psychopathy, PTSD, anxiety, and other disorders (Veit et al., 2013; VanElzakker et al., 2014).”
Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior
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“…behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022; Kietzman and Gourley, 2023).”
Elevated fetal steroidogenic activity in autism
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Social brain, social dysfunction and social withdrawal
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“…neuropeptide signaling, neurogenesis, synaptic programming, and cell differentiation, migration, and death are in fl uenced by gonadal hormones during development and may be involved in the social and fear memory de fi cits (Baron-Cohen et al., 2005, 2011; Schaafsma et al., 2017; Ferri et al., 2018).”
Self-citationThe 2nd to 4th digit ratio and autism
Manning, J. T., Baron‐Cohen, S., Wheelwright, S. J., & Sanders, G. (2001) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2001.tb00181.x · Cited by 391 · cited 2× · see citing works
“…in amniotic fl uid, maternal blood, and cord blood, with ASD-relevant traits or increased likelihood of neurodevelopmental disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006;…”
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“…blood, with ASD-relevant traits or increased likelihood of neurodevelopmental disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al.,…”
The amygdala as a hub in brain networks that support social life
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“…memory behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022; Kietzman and Gourley,…”
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“In rodents, sex hormone-mediated effects on brain development are complete by Postnatal Day (PN)10 (Davis et al., 1996; McCarthy et al., 2018).”
InfluentialFoetal testosterone and eye contact in 12-month-old human infants
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“…uid, maternal blood, and cord blood, with ASD-relevant traits or increased likelihood of neurodevelopmental disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010,…”
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“Many social behaviors exhibit sex differences and are sensitive to gonadal hormones and endocrine disruptors (Bell, 2018).”
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Topical Review: Fetal Testosterone and Sex Differences in Typical Social Development and in Autism
Knickmeyer, R. C., & Baron-Cohen, S. (2006) · Journal of Child Neurology · doi:10.1177/08830738060210101601 · Cited by 230 · cited 1× · see citing works
“…likelihood of neurodevelopmental disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al.,…”
Foetal testosterone and vocabulary size in 18- and 24-month-old infants
Lutchmaya, S., Baron‐Cohen, S., & Raggatt, P. R. (2001) · Infant Behavior and Development · doi:10.1016/s0163-6383(02)00087-5 · Cited by 225 · cited 2× · see citing works
“…uid, maternal blood, and cord blood, with ASD-relevant traits or increased likelihood of neurodevelopmental disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010,…”
Foetal testosterone and autistic traits in 18 to 24-month-old children
Auyeung, B., Taylor, K., Hackett, G., & Baron-Cohen, S. (2010) · Molecular Autism · doi:10.1186/2040-2392-1-11 · Cited by 208 · cited 1× · see citing works
“…disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al., 2021; Firestein et al., 2022).”
van de Beek, C., Thijssen, J. H. H., Cohen‐Kettenis, P. T., van Goozen, S. H. M., & Buitelaar, J. K. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.06.010 · Cited by 203 · see citing works
Baron-Cohen, S., Tsompanidis, A., Auyeung, B., Nørgaard-Pedersen, B., Hougaard, D. M., Abdallah, M., Cohen, A., & Pohl, A. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0454-9 · Cited by 200 · see citing works
Solié, C., Girard, B., Righetti, B., Tapparel, M., & Bellone, C. (2022) · Nature Neuroscience · doi:10.1038/s41593-021-00972-9 · Cited by 186 · cited 1× · see citing works
“The ventral tegmental area, nucleus accumbens, and cerebellum have also been implicated in the regulation of social behavior (Gunaydin et al., 2014; Carta et al., 2019; Porcelli et al., 2019; Musardo et al., 2022; Solié et al., 2022).”
Female reproduction and type 1 diabetes: From mechanisms to clinical findings
Codner, E., Merino, P. M., & Tena-Sempere, M. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms024 · Cited by 182 · cited 1× · see citing works
“…including congenital adrenal hyperplasia, polycystic ovarian syndrome (PCOS), pre-eclampsia, maternal diabetes, and maternal stress (Lai et al., 2011; Codner et al., 2012; Kumar et al., 2018; Xiang et al., 2018; Gumusoglu et al., 2020; Rowland and Wilson, 2021; Li et al., 2023; Meng et al., 2023).”
Etiologies underlying sex differences in autism spectrum disorders
Schaafsma, S. M., & Pfaff, D. W. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.006 · Cited by 178 · cited 1× · see citing works
“…an interaction of genes or environmental insults and sex hormone levels likely contribute to the development of neuropsychiatric conditions, and there is some evidence of this (Schaafsma and Pfaff, 2014; Young and Pfaff, 2014; Baron-Cohen et al., 2015; Schaafsma et al., 2017; Bordt et al., 2024).”
Neurodevelopmental Outcomes of Prenatal Preeclampsia Exposure
Gumusoglu, S. B., Chilukuri, A. S. S., Santillan, D. A., Santillan, M. K. O., & Stevens, H. E. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.02.003 · Cited by 162 · cited 1× · see citing works
“…including congenital adrenal hyperplasia, polycystic ovarian syndrome (PCOS), pre-eclampsia, maternal diabetes, and maternal stress (Lai et al., 2011; Codner et al., 2012; Kumar et al., 2018; Xiang et al., 2018; Gumusoglu et al., 2020; Rowland and Wilson, 2021; Li et al., 2023; Meng et al., 2023).”
Frye, R. E. (2018) · CNS Drugs · doi:10.1007/s40263-018-0556-y · Cited by 157 · cited 1× · see citing works
“Social behavior is disrupted in ASD, ADHD, schizophrenia, PTSD, psychopathy, and others (Nijmeijer et al., 2008; Kennedy and Adolphs, 2012; Homberg et al., 2016; Frye, 2018; Porcelli et al., 2019; Scoglio et al., 2022).”
Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · cited 1× · see citing works
“The de fi cits were also not attributed to heightened anxiety-like behavior, which can co-occur with social de fi cits (Allsop et al., 2014; Felix-Ortiz et al., 2016).”
Milne, E., White, S., Campbell, R., Swettenham, J., Hansen, P., & Ramus, F. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-0052-3 · Cited by 144 · cited 1× · see citing works
“…disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al., 2021; Firestein et al., 2022).”
Estrogen involvement in social behavior in rodents: Rapid and long-term actions
Ervin, K. S. J., Lymer, J., Matta, R., Clipperton‐Allen, A. E., Kavaliers, M., & Choleris, E. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.023 · Cited by 135 · cited 1× · see citing works
“…social de fi cits, and a single-nucleotide polymorphism was reported to correlate with severity in social interaction de fi cits in a group of children with autism, although ESR1 is not considered a high con fi dence risk gene for ASD (Ervin et al., 2015; Doi et al., 2018; Enriquez et al., 2021).”
Sex-specific gene–environment interactions underlying ASD-like behaviors
Schaafsma, S. M., Gagnidze, K., Reyes, A., Norstedt, N., Månsson, K., Francis, K., & Pfaff, D. W. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619312114 · Cited by 126 · see citing works
de Bruin, E. I., Verheij, F., Wiegman, T., & Ferdinand, R. F. (2006) · Developmental Medicine & Child Neurology · doi:10.1017/s0012162206002118 · Cited by 124 · see citing works
Davies, W. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.003 · Cited by 122 · see citing works
Ghahramani, N. M., Ngun, T. C., Chen, P.-Y., Tian, Y., Krishnan, S., Muir, S., Rubbi, L., Arnold, A. P., de Vries, G. J., Forger, N. G., et al. (2014) · Biology of Sex Differences · doi:10.1186/2042-6410-5-8 · Cited by 121 · cited 3× · see citing works
“…oil, a dose previously shown to induce brain masculinization in a female rodent; Goel and Bale, 2008; Hisasue et al., 2010; Seney et al., 2012; Ghahramani et al., 2014; Nakachi et al., 2015) or veh (20 µl sesame oil) was administered subcutaneously at one of two timepoints: to pups on the day…”
Maternal Type 1 Diabetes and Risk of Autism in Offspring
Xiang, A. H., Wang, X., Martinez, M. P., Page, K. A., Buchanan, T. A., & Feldman, R. K. (2018) · JAMA · doi:10.1001/jama.2018.7614 · Cited by 121 · cited 1× · see citing works
“…including congenital adrenal hyperplasia, polycystic ovarian syndrome (PCOS), pre-eclampsia, maternal diabetes, and maternal stress (Lai et al., 2011; Codner et al., 2012; Kumar et al., 2018; Xiang et al., 2018; Gumusoglu et al., 2020; Rowland and Wilson, 2021; Li et al., 2023; Meng et al., 2023).”
The association between gestational diabetes and ASD and ADHD: a systematic review and meta-analysis
Rowland, J., & Wilson, C. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-84573-3 · Cited by 120 · see citing works
Goel, N., & Bale, T. L. (2008) · Endocrinology · doi:10.1210/en.2008-0433 · Cited by 109 · cited 4× · see citing works
“T propionate (Sigma-Aldrich; 100 µg in 20 µl sesame oil, a dose previously shown to induce brain masculinization in a female rodent; Goel and Bale, 2008; Hisasue et al., 2010; Seney et al., 2012; Ghahramani et al., 2014; Nakachi et al., 2015) or veh (20 µl sesame oil) was administered…”
InfluentialAndrogens in maternal vascular and placental function: implications for preeclampsia pathogenesis
Kumar, S., Gordon, G. H., Abbott, D. H., & Mishra, J. S. (2018) · Reproduction · doi:10.1530/rep-18-0278 · Cited by 109 · cited 1× · see citing works
“…including congenital adrenal hyperplasia, polycystic ovarian syndrome (PCOS), pre-eclampsia, maternal diabetes, and maternal stress (Lai et al., 2011; Codner et al., 2012; Kumar et al., 2018; Xiang et al., 2018; Gumusoglu et al., 2020; Rowland and Wilson, 2021; Li et al., 2023; Meng et al., 2023).”
Auyeung, B., Ahluwalia, J., Thomson, L., Taylor, K., Hackett, G., O’Donnell, K. J., & Baron-Cohen, S. (2012) · Molecular Autism · doi:10.1186/2040-2392-3-17 · Cited by 106 · cited 1× · see citing works
“…disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al., 2021; Firestein et al., 2022).”
Fast, furious and enduring: Sensitive versus critical periods in sexual differentiation of the brain
McCarthy, M. M., Herold, K., & Stockman, S. L. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.10.030 · Cited by 97 · cited 4× · see citing works
“In rodents, sex hormone-mediated effects on brain development are complete by Postnatal Day (PN)10 (Davis et al., 1996; McCarthy et al., 2018).”
InfluentialThy1-Expressing Neurons in the Basolateral Amygdala May Mediate Fear Inhibition
Jasnow, A. M., Ehrlich, D., Choi, D. C., Dabrowska, J., Bowers, M. E., McCullough, K. M., Rainnie, D. G., & Ressler, K. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5539-12.2013 · Cited by 92 · cited 1× · see citing works
“…both social and fear memory behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022;…”
Sociability Deficits and Altered Amygdala Circuits in Mice Lacking Pcdh10, an Autism Associated Gene
Schoch, H., Kreibich, A. S., Ferri, S. L., White, R. S., Bohorquez, D., Banerjee, A., Port, R. G., Dow, H. C., Cordero, L., Pallathra, A. A., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.06.008 · Cited by 92 · cited 1× · see citing works
“…as neonates (no neonatal injection); both social preference indices at ∼ PN30 and 24 h fear memory results at ∼ PN60 were comparable between mice administered veh and never-injected control mice we have collected over various experiments (Schoch et al., 2017; Ferri et al., 2016, 2020, 2021).”
Self-citationSex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 89 · cited 1× · see citing works
“Numerous sex differences in morphology and function in these brain regions have been documented, including in area volume, cell number, size, and structure, and most express androgen and estrogen receptors (Premachandran et al., 2020).”
Homberg, J. R., Kyzar, E. J., Nguyen, M., Norton, W., Pittman, J. T., Poudel, M. K., Gaikwad, S., Nakamura, S., Koshiba, M., Yamanouchi, H., et al. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.013 · Cited by 83 · cited 1× · see citing works
“Social behavior is disrupted in ASD, ADHD, schizophrenia, PTSD, psychopathy, and others (Nijmeijer et al., 2008; Kennedy and Adolphs, 2012; Homberg et al., 2016; Frye, 2018; Porcelli et al., 2019; Scoglio et al., 2022).”
Social Functioning in Individuals With Post-Traumatic Stress Disorder: A Systematic Review
Scoglio, A. A. J., Reilly, E. D., Girouard, C. M., Quigley, K. S., Carnes, S., & Kelly, M. M. (2020) · Trauma Violence & Abuse · doi:10.1177/1524838020946800 · Cited by 80 · see citing works
Hisasue, S.-I., Seney, M. L., Immerman, E., & Forger, N. G. (2010) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01669.x · Cited by 78 · see citing works
Oxytocin neurons mediate the effect of social isolation via the VTA circuits
Musardo, S., Contestabile, A., Knoop, M., Baud, O., & Bellone, C. (2022) · eLife · doi:10.7554/elife.73421 · Cited by 77 · cited 1× · see citing works
“The ventral tegmental area, nucleus accumbens, and cerebellum have also been implicated in the regulation of social behavior (Gunaydin et al., 2014; Carta et al., 2019; Porcelli et al., 2019; Musardo et al., 2022; Solié et al., 2022).”
Prevalence of neurodevelopmental disorders among US children and adolescents in 2019 and 2020
Yang, Y., Zhao, S., Zhang, M., Xiang, M., Zhao, J., Chen, S., Wang, H., Han, L., & Ran, J. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.997648 · Cited by 76 · see citing works
Optogenetic dissection of amygdala functioning
LaLumiere, R. T. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00107 · Cited by 71 · cited 1× · see citing works
“…behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022; Kietzman and Gourley, 2023).”
Park, B. Y., Lee, B. K., Burstyn, I., Tabb, L. P., Keelan, J. A., Whitehouse, A., Croen, L., Fallin, M. D., Hertz‐Picciotto, I., Montgomery, O. C., et al. (2017) · Molecular Autism · doi:10.1186/s13229-017-0118-z · Cited by 61 · cited 1× · see citing works
“…disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al., 2021; Firestein et al., 2022).”
Sex differences in neurological and psychiatric disorders
Young, L. J., & Pfaff, D. W. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.05.005 · Cited by 59 · cited 1× · see citing works
“…an interaction of genes or environmental insults and sex hormone levels likely contribute to the development of neuropsychiatric conditions, and there is some evidence of this (Schaafsma and Pfaff, 2014; Young and Pfaff, 2014; Baron-Cohen et al., 2015; Schaafsma et al., 2017; Bordt et al., 2024).”
Deficient fear conditioning in psychopathy as a function of interpersonal and affective disturbances
Veit, R., Konicar, L., Klinzing, J. G., Barth, B., Yilmaz, Ö., & Birbaumer, N. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00706 · Cited by 53 · see citing works
Age- and sex-specific fear conditioning deficits in mice lacking Pcdh10, an Autism Associated Gene
Ferri, S. L., Dow, H. C., Schoch, H., Lee, J. Y., Brodkin, E. S., & Abel, T. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107364 · Cited by 51 · see citing works
Self-citationHippocampus and amygdala fear memory engrams re-emerge after contextual fear relapse
Zaki, Y., Mau, W., Cincotta, C., Monasterio, A., Odom, E. I., Doucette, E., Grella, S. L., Merfeld, E., Shpokayte, M., & Ramirez, S. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01407-0 · Cited by 49 · cited 1× · see citing works
“…behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022; Kietzman and Gourley, 2023).”
Activation of basolateral amygdala in juvenile C57BL/6J mice during social approach behavior
Ferri, S. L., Kreibich, A. S., Torre, M., Piccoli, C. T., Dow, H. C., Pallathra, A. A., Li, H., Bilker, W. B., Gur, R. C., Abel, T. G., et al. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.08.006 · Cited by 48 · see citing works
Self-citationPrenatal androgen-receptor activity has organizational morphological effects in mice
Huber, S. E., Lenz, B., Kornhuber, J., & Müller, C. P. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188752 · Cited by 46 · cited 1× · see citing works
“Prenatal manipulation of androgen receptor activity in mice has also been shown to produce sex-speci fi c morphological outcomes relevant to those observed in humans, such as digit ratio and body morphology (Huber et al., 2017).”
Neonatal testosterone partially organizes sex differences in stress-induced emotionality in mice
Seney, M. L., Walsh, C., Stolakis, R., & Sibille, E. L. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.02.014 · Cited by 32 · see citing works
Huber, S. E., Zoicas, I., Reichel, M., Mühle, C., Büttner, C., Ekici, A. B., Eulenburg, V., Lenz, B., Kornhuber, J., & Müller, C. P. (2017) · Addiction Biology · doi:10.1111/adb.12540 · Cited by 30 · see citing works
Kietzman, H. W., & Gourley, S. L. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105075 · Cited by 30 · cited 1× · see citing works
“…behavior and may be disrupted by excess T early in development (Maren, 2001; Kim and Jung, 2006; Marschner et al., 2008; Jasnow et al., 2013; Bickart et al., 2014; Felix-Ortiz and Tye, 2014; LaLumiere, 2014; Bicks et al., 2015; Kim et al., 2016; Zaki et al., 2022; Kietzman and Gourley, 2023).”
Hatanaka, Y., Wada, K., & Kabuta, T. (2015) · Neurochemistry International · doi:10.1016/j.neuint.2015.04.008 · Cited by 22 · cited 1× · see citing works
“…utero; one found that males, but not females, exhibited increased density, instability, and abnormal morphology in dendritic spines of the frontal cortex, and another showed male-speci fi c decreases in corticosterone response following restraint stress (Hatanaka et al., 2015; Wilson et al., 2020).”
Firestein, M. R., Romeo, R. D., Winstead, H., Goldman, D. A., Grobman, W. A., Haas, D., Mercer, B., Parker, C., Parry, S., Reddy, U., et al. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105125 · Cited by 22 · see citing works
Doi, H., Fujisawa, T. X., Iwanaga, R., Matsuzaki, J., Kawasaki, C., Tochigi, M., Sasaki, T., Kato, N., & Shinohara, K. (2018) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2018.02.014 · Cited by 21 · cited 1× · see citing works
“…social de fi cits, and a single-nucleotide polymorphism was reported to correlate with severity in social interaction de fi cits in a group of children with autism, although ESR1 is not considered a high con fi dence risk gene for ASD (Ervin et al., 2015; Doi et al., 2018; Enriquez et al., 2021).”
Bordt, E. A., Moya, H., Jo, Y. C., Ravichandran, C. T., Bankowski, I. M., Ceasrine, A. M., McDougle, C. J., Carlezon, W. A., & Bilbo, S. D. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.11.010 · Cited by 20 · see citing works
Signaling Pathways and Sex Differential Processes in Autism Spectrum Disorder
Enriquez, K., Gupta, A. R., & Hoffman, E. J. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.716673 · Cited by 19 · cited 2× · see citing works
“…social de fi cits, and a single-nucleotide polymorphism was reported to correlate with severity in social interaction de fi cits in a group of children with autism, although ESR1 is not considered a high con fi dence risk gene for ASD (Ervin et al., 2015; Doi et al., 2018; Enriquez et al., 2021).”
Prenatal Sex Hormone Exposure Is Associated with the Development of Autism Spectrum Disorder
Li, M., Usui, N., & Shimada, S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032203 · Cited by 19 · see citing works
Association between sex steroid hormones and subsequent hyperglycemia during pregnancy
Meng, Y., Thornburg, L. L., Hoeger, K. M., Rivera‐Núñez, Z., Kautz, A., Evans, A. T., Wang, C., Miller, R. K., Groth, S. W., O’Connor, T. G., et al. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1213402 · Cited by 18 · cited 1× · see citing works
“…including congenital adrenal hyperplasia, polycystic ovarian syndrome (PCOS), pre-eclampsia, maternal diabetes, and maternal stress (Lai et al., 2011; Codner et al., 2012; Kumar et al., 2018; Xiang et al., 2018; Gumusoglu et al., 2020; Rowland and Wilson, 2021; Li et al., 2023; Meng et al., 2023).”
Sociability development in mice with cell-specific deletion of the NMDA receptor NR1 subunit gene
Ferri, S. L., Pallathra, A. A., Kim, H., Dow, H. C., Raje, P., McMullen, M., Bilker, W. B., Siegel, S. J., Abel, T., & Brodkin, E. S. (2020) · Genes, Brain and Behavior · doi:10.1111/gbb.12624 · Cited by 15 · cited 1× · see citing works
“…as neonates (no neonatal injection); both social preference indices at ∼ PN30 and 24 h fear memory results at ∼ PN60 were comparable between mice administered veh and never-injected control mice we have collected over various experiments (Schoch et al., 2017; Ferri et al., 2016, 2020, 2021).”
Self-citationA lumpers versus splitters approach to sexual differentiation of the brain
McCarthy, M. M. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.004 · Cited by 14 · cited 3× · see citing works
“Females of those species are exposed to signi fi cantly lower levels of gonadal hormones during early development (Gillies and McArthur, 2010; McCarthy, 2011).”
Dib, T., Martínez-Pinto, J., Reyes-Parada, M. I., Torres, G. E., & Sotomayor‐Zárate, R. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.001 · Cited by 12 · cited 1× · see citing works
“…exposure to androgens alters neurochemistry and produces sex-speci fi c behavioral outcomes, including those related to reward sensitivity, such as alcohol drinking and amphetamine-and methylphenidate-induced locomotor activity (Dib et al., 2018; Huber et al., 2018; Elgueta-Reyes et al., 2022).”
McKenna, B. G., Huang, Y., Vervier, K., Hofammann, D., Cafferata, M., Al-Momani, S., Lowenthal, F., Zhang, A., Koh, J.-Y., Thenuwara, S., et al. (2021) · Molecular Autism · doi:10.1186/s13229-021-00450-w · Cited by 11 · cited 1× · see citing works
“…disorder diagnosis (Manning et al., 2001; Lutchmaya et al., 2002a,b; Chapman et al., 2006; De Bruin et al., 2006; Knickmeyer and Baron-Cohen, 2006; Milne et al., 2006; Auyeung et al., 2010, 2012; Baron-Cohen et al., 2015; Park et al., 2017; McKenna et al., 2021; Firestein et al., 2022).”
Wilson, H. A., Martin, E. R., Howes, C., Wasson, C. S., Newman, A. E. M., Choleris, E., & MacLusky, N. J. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146613 · Cited by 8 · cited 1× · see citing works
“…utero; one found that males, but not females, exhibited increased density, instability, and abnormal morphology in dendritic spines of the frontal cortex, and another showed male-speci fi c decreases in corticosterone response following restraint stress (Hatanaka et al., 2015; Wilson et al., 2020).”
Kalinichenko, L. S., Smaga, I., Filip, M., Lenz, B., Kornhuber, J., & Müller, C. P. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114225 · Cited by 8 · cited 1× · see citing works
“…injections in pregnant dams increased brain T levels in male fetuses and led to male-speci fi c changes in N -methyl- D -aspartate receptor subunit expression, a pathway implicated in both social behavior and neurodevelopmental disorders (Kalinichenko et al., 2023; Brown et al., 2024).”
Elgueta-Reyes, M., Velásquez, V. B., Espinosa, P., Riquelme, R., Dib, T., Sanguinetti, N. K., Escobar, A. P., Martínez-Pinto, J., Renard, G. M., & Sotomayor‐Zárate, R. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126575 · Cited by 5 · see citing works
Nakachi, Y., Iseki, M., Yokoo, T., Mizuno, Y., & Okazaki, Y. (2015) · The Journal of Sexual Medicine · doi:10.1111/jsm.12802 · Cited by 4 · see citing works
Serine racemase deletion alters adolescent social behavior and whole-brain cFos activation
Brown, S. E., Wang, Z., Newman, E. L., Engin, E., Berretta, S., Balu, D. T., & Folorunso, O. O. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1365231 · Cited by 3 · cited 1× · see citing works
“…injections in pregnant dams increased brain T levels in male fetuses and led to male-speci fi c changes in N -methyl- D -aspartate receptor subunit expression, a pathway implicated in both social behavior and neurodevelopmental disorders (Kalinichenko et al., 2023; Brown et al., 2024).”
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Zhang, Y., Huang, M., Duan, R., Huang, W., & Tan, Z. (2025) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2025.118287 · Cited by 3 · see citing works
Disruption of DNA Repair as an Emerging Epigenetic Mechanism Underlying Autism Spectrum Disorder
Kelvington, B. A., Kim, J., Banerjee, S., Stevens, H. E., Chow, H., & Abel, T. G. (2026) · Current Psychiatry Reports · doi:10.1007/s11920-026-01684-2
Ju, L.-S., Khan, Z., Gravenstein, N. L., Setlow, B., & Martynyuk, A. E. (2026) · Anesthesia & Analgesia · doi:10.1213/ane.0000000000008197
Zhang, Y., & Zhang, L. (2026) · Frontiers in Public Health · doi:10.3389/fpubh.2026.1860897
“However, such biological pathways remain unconfirmed within the current small sample and require targeted mechanistic research for validation (31–32).”
- Authors
- Quiñones-Labernik, P., Blocklinger, K. L., Bruce, M. R., Hagan, E., Preuschl, D., Tesar, C., & Ferri, S. L.
- Affiliations
- University of Iowa (US)
- Temple University (US)
- Venue
- eneuro
- Publisher
- Society for Neuroscience
- Published
- 2025-07-07
- Volume
- 12
- Issue
- 8
- Pages
- ENEURO.0020-25.2025
- ISSN
- 2373-2822 (ISSN-L)
- PMC
- PMC10614869
- OpenAlex
- W4412075488
- Semantic Scholar
- e5a29eb29490543cec41a1b61af92d78a6dad57b
- Cited by
- 4
- References
- 85
- Citations by year
- 2026: 3 · 2025: 1
- FWCI
- 1.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eNeuro (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by-nc-nd)
- PubMed Central (submittedVersion, cc-by)
- Funders
- HHS | NIH | National Institute of Mental Health (K01 MH119540)
- HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (P50 HD103556)
- HHS | NIH | National Institute of General Medical Sciences (T32 GM144636)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- neonatal testosterone, social approach behavior, contextual fear memory, brain masculinization, critical periods of development, gonadal hormones, wild-type mice
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.
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