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Neuroethics (2013) 6:369–409

DOI 10.1007/s12152-012-9169-1

ORIGINAL PAPER

Is There Neurosexism in Functional Neuroimaging


Investigations of Sex Differences?
Cordelia Fine

Received: 1 May 2012 / Accepted: 15 October 2012 / Published online: 7 December 2012
# Springer Science+Business Media Dordrecht 2012

Abstract The neuroscientific investigation of sex dif- toward the presentation of sex differences in the brain
ferences has an unsavoury past, in which scientific as extensive, functionally significant, and fixed—and
claims reinforced and legitimated gender roles in ways therefore implicitly supportive of a gender essentialist
that were not scientifically justified. Feminist critics perspective. It is suggested that taking feminist
have recently argued that the current use of functional criticisms into account would bring about substantial
neuroimaging technology in sex differences research improvement in the quality of the science, as well as a
largely follows that tradition. These charges of ‘neuro- reduction in socially harmful consequences.
sexism’ have been countered with arguments that the
research being done is informative and valuable and Keywords Sex/gender . fMRI . Gender stereotypes .
that an over-emphasis on the perils, rather than the Publication bias . Gender essentialism . Citation bias
promise, of such research threatens to hinder scientific
progress. To investigate the validity of these contrast-
ing concerns, recent functional magnetic resonance Introduction
imaging (fMRI) investigations of sex differences and
citation practices were systematically examined. In A now notorious claim of Victorian sexual science was
line with the notion of neurosexism, the research was that men’s intellectual superiority could be explained by
found to support the influence of false-positive claims the larger male brain—a phenomenon described by one
of sex differences in the brain, to enable the prolifer- scientist as the “missing five ounces” of female brain [1,
ation of untested, stereotype-consistent functional p. 23]. Developed under the assumption of a positive
interpretations, and to pay insufficient attention to correlation between brain size and intelligence, it was
the potential plasticity of sex differences in both brain only abandoned some time after the absence of such a
and mind. This, it is argued, creates a literature biased relation became clear [see 2]. Historical examples of
erroneous hypotheses regarding the neurological differ-
ences between the sexes and their functional implica-
C. Fine
tions are readily found [2–4], and it is not controversial
Psychological Sciences, University of Melbourne,
Parkville, Australia to suggest that such scientific claims had political influ-
ence. Russett, for instance, has argued that the theories
C. Fine (*) of the Victorian sexual scientists were not simply gar-
Centre for Ethical Leadership, Melbourne Business School,
nered as support by those who opposed greater social
200 Leicester Street,
Carlton, Victoria 3053, Australia equality for the sexes, but were a “key source” of that
e-mail: cfine@unimelb.edu.au opposition [2, p. 191].
370 C. Fine

In recent decades, a new research tool has been endorsed by some within the scientific community is
made available to those interested in neurological dif- that the hypothesis that there are intrinsic sex differences
ferences between the sexes: functional neuroimaging in brain and behavior is ‘politically incorrect’: it has
(FNI). While neuroscientists have long been able to been described by a number of scientists as “politically
compare structural features of the male and female dangerous” [25, p. xi], “taboo” [26, p. 19, 27] and,
brain, technologies such as functional magnetic reso- politically, “not a permissible hypothesis” [Haidt, quot-
nance imaging (fMRI) and (now less commonly) pos- ed in 28]. In a similar vein, at a recent Social Issues
itron emission tomography (PET) can indirectly index Roundtable on the ‘The Promise and Peril of Research
neuronal activity in the working brain. Following in- on Sex Differences’ at the 2011 meeting of the Society
sightful and important critiques of structural neurosci- for Neuroscience, Cahill [quoted in 29] was reported as
entific research by feminist neurobiologists [e.g., 5–8], raising “the opposite concern [to the abuse of neurosci-
the use of FNI to investigate sex differences has also ence to justify sexism]: His colleagues are so afraid of
recently begun to be subjected to feminist scrutiny. A being called ‘neurosexists’ that they’ve refused to study
number of scholars have argued that, as in the past, or acknowledge differences.”
FNI research currently reinforces and legitimates tra- This article seeks to gain insight into the validity of
ditional gender stereotypes and roles in ways that are these differing perspectives by using recent two year
not scientifically justified. The growing number of literature samples and a case study to investigate how
charges of ‘neurosexism’ (as it was first termed in this researchers address three substantial obstacles to gain-
journal [9]) have argued for bias in the way FNI ing replicable and valuable insights into sex differ-
research on sex differences is conducted and inter- ences from FNI data. The first difficulty is the scope
preted, detrimental effects for understanding the com- for false-positive errors that arises when sex compar-
plex phenomenon of gender, as well as harmful social isons are made. The second obstacle lies in under-
and psychological effects from the reification of gender standing what, if anything, a sex difference in brain
roles [e.g., Fine, C. unpublished. Neurosexism in func- activity means in terms of differences in mental pro-
tional neuroimaging: from scanner to pseudoscience to cesses. Group differences in brain activity are not
psyche. In The Sage handbook of gender and psychol- readily translated into psychological differences and
ogy, eds. M. Ryan and N. Branscombe. Thousand Oaks: this gap in knowledge of brain-mind relations creates a
Sage., 10–18]. danger that, as in the past, gender stereotypes will be
However, a stark counterpoint to this perspective is drawn upon to putty-fill in the gap [6]. The third issue
that there are “deeply entrenched, harmful, and general- is that sex differences in both brain and behavior are
ly implicit biases against sex influence research among potentially malleable, or plastic, meaning that insight
neuroscientists” [19, p. 38]. Recent criticisms of re- into the developmental or situational origins of sex
search investigating neurobiological contributions to differences in the brain, and the extent to which social
sex differences [10, 20] have been countered with argu- factors increase, reduce, eliminate or even reverse
ments that there is “an overemphasis on criticism of a them, cannot be gained through single “snap-shot”
few errant studies or errant interpretations”, and that comparisons of male and female brains [18]. Inade-
they do not make sufficient acknowledgment of the quate treatment of these difficulties creates potential
careful and valuable neuroscientific research into sex for a bias toward an exaggeration of the extensiveness,
differences that is being conducted [21, 22, p. 3]. From functional importance, and fixedness of sex differen-
this perspective, the foremost concern is that failure to ces in the brain. Such a presentation would implicitly
investigate sex influences on the brain impedes scientif- support gender essentialism; that is the notion of deep-
ic progress in understanding sex differences in behavior rooted, permanent, and distinct male versus female
and vulnerability to psychiatric and developmental dis- “essences” that make gender divisions seem natural,
orders [e.g., 19, 23, 24], and that an over-emphasis on inevitable, and desirable [for overview of theory and
the perils, rather than the promise, of such research will data on psychological essentialism, see 30]. Alterna-
hinder scientific progress. Thus McCarthy & Ball [22, tively, if charges of neurosexism are incorrect, then the
p. 3] expressed fear that recent feminist critiques “threat- overall research picture (excepting the possibility of a
en to severely hamper or even reverse the progress being few isolated ‘bad apples’) should reveal methods and
made in this field”. It is worth noting that a perception practices that take care to reduce the influence of false-
Is there Neurosexism in Functional Neuroimaging? 371

positive errors on the field, that involve the systematic “natural default” and “seemingly effortless and obvi-
testing of hypotheses about the functional implications ous in brain research” [12, p. 54]. They have also
of sex differences in the brain in order to reduce scope noted that, in comparisons of pathological groups with
for gendered assumptions to creep into interpretations, controls, “introducing sex/gender as a supplementary
and that show careful attention to the influence of factor augments the possibilities for differentiating the
gendered experiences on sex differences in brain groups from each other”, offering additional opportu-
activity. nities for publishing.
A second reason for concern regarding false-
positive findings in FNI investigations of sex differ-
Exaggeration of Extent of Male/Female Brain ences arises from the small sample sizes that are
Activation Differences? Sex Comparisons common in FNI research. As Wallentin [37] has noted
and False-Positive Errors in relation to sex difference findings, FNI studies are
especially vulnerable to spurious results due to the
There can be legitimate reasons to compare the sexes difficulty of balancing participants on nuisance varia-
in FNI work [see 24]. For example, if male and female bles (like breathing rate and caffeine intake) that affect
samples differ behaviorally, for whatever reason, sex the imaging signal, and that this is particularly an issue
differences in brain activity can be expected. It is also when sample sizes are small. An analysis of the effect
possible that males and females may reach the same of sample size on the reliability and sensitivity of
behavioral end via different neural means [31–33]. If fMRI studies concluded that the large inter-subject
so, conflating the two populations, or only investigat- variability is a key issue, and recommended a sample
ing one sex and extrapolating to the other sex, may be size of at least twenty for adequate reliability in group
inappropriate. Indeed, one rationale for making sex fMRI studies [38]. To the extent that sex comparisons
comparisons in neuroscientific research is to redress are made post hoc rather than a priori, the issue of
an historical tendency for biological research to be sample size is likely to be exacerbated further, as
conducted mostly on males, with findings and impli- researchers will not have considered in advance the
cations for pathology then extrapolated, perhaps incor- number of male and female participants necessary for
rectly, to females [24]. However, publication bias adequate statistical power (sensitivity) or reliability.
towards statistically significant findings is a long- In addition, the choices researchers make about
noted problem within sex differences research [34]. how to analyse their results can increase the scope
When a single experiment establishes a “significant for false-positive errors in sex comparisons. For the
difference” between the sexes, this does not necessar- purposes of analysis, the brain is divided into tens of
ily reflect a real and reliable result. False-positive thousands of tiny regions (or voxels), and tested for
errors and publication bias is a major issue in behav- blood flow changes as a function of the psychological
ioral science generally [for recent discussions, see 35, construct of interest. Brain regions that show changed
36]. However, this problem can be especially exacer- activity become plausible (although far from certain)
bated in sex differences research. The primary reason candidates for involvement in the psychological pro-
is the ease and obviousness of testing for sex differ- cess of interest. As Bluhm [15] and Kaiser et al. [12]
ences, even in the absence of an a priori reason to do have noted, researchers may sometimes inappropriate-
so. Since by convention one in twenty “significant” ly make use of within-group analyses to make claims
results occur by chance, if 20 researchers routinely test about male/female difference. That is, researchers may
for sex differences then, even if there is no real differ- analyze data for males and females separately and find
ence between the populations, one researcher will find that while a particular brain region was, say, significant-
a statistically significant difference. ly activated in males in the experimental task (compared
There is no way of knowing whether researchers with a control condition), this difference was not statis-
who do not report sex comparisons have nonetheless tically significant in females. However, within-group
tested for them, and it is not known how common such analyses do not allow claims to be made about
practices are. However, Kaiser and colleagues have between-group differences. (In this hypothetical exam-
argued that because sex is a primary and ubiquitous ple, it is possible that male/female activity in that par-
social category, classifying participants by sex is a ticular brain region does not significantly differ.)
372 C. Fine

Despite this, within-group analyses have been found to differences research, then this will be reflected in the
be surprisingly common in neuroscience research [39]. literature. This was systematically investigated in three
The reality of the problem of false-positive errors in ways: first, by looking at typical sample sizes in stud-
FNI studies of sex differences is well-illustrated by ies reporting sex differences in brain activation; sec-
investigations of the long-standing idea that the male ond, by assessing the standards of evidence deemed
brain is more lateralized than the female brain for sufficient for a hypothesis of male/female brain differ-
language processing: that is, that the male brain tends ence to be presented as supported in the scientific
to engage the left hemisphere when processing lan- literature; and third, by examining carefulness in citing
guage stimuli, while the female brain tends to engage a potentially spurious result.
both. This alleged sex difference in lateralization is
often suggested to underlie female language superior- Typical Sample Sizes
ity, and a similar lateralization difference for visuo-
spatial processing to underlie male superiority in that Typical sample sizes for FNI studies reporting sex
domain [see 8, 10, 40] In an oft-cited fMRI study of 19 differences offer an insight into the treatment of scope
men and 19 women, Shaywitz and colleagues found for false-positive errors in this area of research. In
that for phonological processing (although not seman- particular, a literature in which studies reporting pos-
tic or orthographic processing), neural activity in lan- itive results are predominantly underpowered, with
guage regions was lateralized in men but not women group sample sizes smaller than twenty [as recommen-
[41]. Yet an investigation of the generalizability of sex ded by 38] or, more liberally, sixteen [as recommen-
differences observed with 13 males and 13 females ded by 46] should create concern that such findings
found that those differences failed to generalize to will not prove to be replicable. Therefore to investi-
similar language tasks within a second group of 10 gate typical sample sizes in this area of research, the
men and 10 women. Moreover, identical analyses of Medline, Web of Science and PsycINFO databases
the same participants ‘discovered’ brain activation were searched for fMRI studies published in 2009
differences between randomly created groups matched and 2010 in which sex differences were referred to in
on sex, performance, and obvious demographic char- the article title.1 Thirty-nine studies fulfilled the nec-
acteristics [42]. Importantly, two recent large meta- essary criteria (see Table 1 and Appendix for further
analyses of FNI studies of language lateralization details).2 Over the entire sample, the mean number of
failed to find evidence overall for sex differences males was 19.0 (median016, sd010.6) and the mean
[43, 44], and the earlier meta-analysis reported mark- number of females was 18.5 (median018, sd09.5).
edly smaller sample sizes for studies reporting sex However, a number of the studies in the sample also
differences (a mean of 31) than for studies reporting made sex-by-group or sex-by-age comparisons, both
no differences (a mean of 76). These findings under- of which require larger sample sizes than for sex-only
line the need for scepticism towards any one particular comparisons, for similar statistical power. For studies
finding of a sex difference, particularly when it arises that made only sex comparisons (n022) the mean
from a small sample. number of males was 13.5 (sd06.4) and the mean
The seriousness of false-positive errors was recent- number of females was 13.8 (sd06.5). It is worth
ly emphasized by Simmons et al. [45, p. 1], who noting that the second largest study in this group (with
suggested that they are “[p]erhaps the most costly a total sample size of 50) reported a null finding [47].
error” in science. They noted that false-positive results For studies reporting sex-by-group comparisons (n0
tend to persist because failures to replicate are incon-
clusive, and unappealing both to attempt by research-
1
This was done using the search terms “sex” or “gender” in
title, and “fMRI”, “functional magnetic resonance imaging” or
ers and to publish by journals. In addition, they can
“functional MRI” in the title, abstract or keywords. ‘Difference’
lead to wasted resources in fruitless research enquiries, was not included as a search term so as to not exclude studies
as well as misguided practical applications. Thus sci- reporting sex/gender similarities. Studies that were not full
entists have general reasons to avoid false-positive reports of original findings that investigated sex differences in
brain activation in humans were then excluded.
errors. If, contra claims of neurosexism, scientists 2
Excluded from the analysis was one study, referred to earlier,
perceive additional political pressures to avoid false- that was specifically testing the generalizability of sex differ-
positive errors (or, indeed, true-positive results) in sex ences based on a total sample size of 20 [42].
Is there Neurosexism in Functional Neuroimaging? 373

Table 1 Numbers of male and female participants in 2009 and 2010 functional MRI studies of sex differences

Study Total Total Subgroups Mean no. males Mean no. females
(by first author name) males females in subgroups in subgroups

Sex only comparison


Aikins 12 12
Cornier 21 22
Domes 16 17
Fine 10 10
Frank 6 6
Garn 13 13
Goldstein 13 12
Ino 10 10
Keller 24 25
Killgore 8 8
Krach 12 12
Lee 12 10
Li 30 30
Mak 12 12
Ohrman 8 12
Owens 9 10
Qiu 19 19
Riedl 10 10
Schmidta 25 25
Straube 12 12
Sveljo 6 6
Wang 10 10
Mean (sd) 13.5 (6.4) 13.8 (6.5)
Sex by group comparison
Bitan 17 22 Low/High VIQ using median split 8.5 11
Clements-Stephens 16 16 Plus/Minus 10 years of age 8 8
Coman 25 18 Genotype 9 12.5
Derntl 12 12 Luteal phase (females) 12 6
Eisenberger 18 18 Treatment versus placebo conditions 9 9
Elsabagh 30 20 Clinical status 15 10
Felmingham 42 44 Trauma exposure and clinical status 14 14.7
Gauthier 22 22 Low/High verbal fluency 11 11
Kempton 40 34 Genotype 13.3 11.3
Klucken 20 20 Awareness of conditioning contingency 10 10
Mather 24 23 Stress versus control conditions 12 11.5
Merz 20 19 Cortisol versus control conditions 10 9.5
Rumberg 12 24 Oral contraceptive status for females 12 12
Valera 46 47 ADHD versus control participants 23 23.5
Mean (sd) 11.9 (3.8) 11.4 (4.1)
Age effects
Christakou 38 25
Rubia 38 25
Zuo 22 29
374 C. Fine

Table 1 (continued)

Study Total Total Subgroups Mean no. males Mean no. females
(by first author name) males females in subgroups in subgroups

Mean (sd) 32.7 (9.2) 26.3 (2.3)


Mean (sd) for entire sample 19.0 (10.6) 18.5 (9.5)
a
This study reported a null result

14) the mean number of males per subgroup was 11.9 case study to assess the standards of evidence required
(sd03.8), and females per subgroup was 11.4 (sd0 to claim a neurological sex difference as supported.
4.0). The largest sample sizes were observed in the This program investigates the proposal that there is a
three studies exploring age effects, for which the mean sex difference in the modulation of memory consoli-
number of males was 32.7 (sd09.2) and the mean dation by the amygdala for emotionally salient mate-
number of females was 26.3 (sd02.3). The distribu- rial [see 19, 48]. Specifically, Cahill and colleagues
tion of sample sizes is shown in Fig. 1, which shows have suggested that there is sex-dependent lateraliza-
that the clear majority of studies had (a mean of) tion of this modulation effect, with the right amygdala
fifteen or fewer participants of each sex in each of more strongly involved in men, and the left in women.
their groups of interest, and that studies were as likely Further theorizing and empirical work has suggested
to have fewer than ten participants as they were to functional implications, such as more enhanced mem-
have more than twenty. It is worth emphasizing that ory for the ‘gist’ of events in males, but of peripheral
these are not studies in which sex differences are information in females [see 19]. For three reasons, this
mentioned incidentally, but studies in which sex dif- claim would appear to be an appropriate and fair test-
ferences are the primary focus of research, as indicated case. First, the hypothesis is based on a well-
by the article title. developed neurocognitive model of emotional memo-
ry enhancement, and predictions regarding sex-
Case Study: Standards of Evidence modulation have been tested in numerous studies. In
other words, it is one of the few examples of a claim of
It might be objected that the above literature survey a sex difference from FNI data that is not based on an
misrepresents the situation, by looking at a sample isolated or post hoc finding. Second, Cahill and col-
made up of largely exploratory and isolated findings leagues have concluded that there is “no reasonable
rather than an established research program. As a test doubt about the existence” of this sex-related laterality
of the validity of this objection, a currently prominent in humans [49, p. 262]. Additionally, the finding has
program of sex differences research was chosen as a been cited without caveat in some subsequent general

Fig. 1 Frequency of 45 Male


male/female group or mean
40 Female
subgroup sample sizes in
2009 and 2010 functional 35
MRI studies of sex
Frequency of 30
differences
male/female 25
group or
subgroup sample 20
sizes
15
10
5
0
<10 10 to 16 to 21 to 26 to 31 to 36 to
15 20 25 30 35 40
Male/female group or mean group sample size
Is there Neurosexism in Functional Neuroimaging? 375

reviews of emotional memory as well those concerned selection bias by including the data of ten female
specifically with sex influences [e.g., 19, 50–52], al- participants from a previous (female only) study
though there are also more cautious review references [58]. Thus, the sample was biased towards supporting
[e.g., 53]. Finally, this research program was described the hypothesis, since it was in part on the basis of
as an example of “high quality research by scientists those data that the hypothesis under test was derived.
who take care in … the scope of their claims”, for This was also the case for the next largest study [55]:
which feminist criticisms of the field are misplaced again, data for eight of the 22 participants came from
[21, p. 1321], reflecting its status as an apparently an earlier (male only) study [54] from which the
well-supported finding. It would therefore appear to hypothesized sex difference was partially derived.
be well-positioned in the literature to have gained The one remaining study that included both males
good empirical support, and thus to be a fair test case and females [49] had only eight men and seven
study for standards of evidence required to claim a women.
finding as supported. Casting further reasonable doubt on the hypothesis
The claim for humans is principally based on FNI is the absence of evidence of sex differences in the
research showing stronger correlations between en- effects of right versus left amygdala damage on emo-
hanced emotional memory assessed at a delay (gener- tional memory in a small patient study [61], and null
ally 2–3 weeks) and right amygdala activity in males, findings in some recent FNI studies of this phenome-
but left amygdala activity in females. Cahill and col- non [62, 63]. Interestingly, Ritchey and colleagues
leagues’ (2004) conclusion that no reasonable doubt [63, p. 2502] argued that their null finding for sex
that this sex-related laterality exists was based on the (noted briefly in the Discussion) “should be treated
finding of the study reported in that article, together with caution … due to relatively small sample sizes for
with six previous studies [54–59]. These seven studies males [n06] and females [n07].” This is a valid point,
are summarized in Table 2, and there are a number of but as noted earlier, such caution is also appropriately
observations to be made. The first point is that four of applied to positive FNI findings from small samples.
the seven studies included only one sex [54, 56, 58, It may be worth stating explicitly that the points
59]. Further, given that the methodologies of these made here should not be taken to imply that the
four studies differed in a number of ways (such as possibility of a sex difference, suggested by the earlier
imaging technology, stimuli, length of delay to mem- findings with male-only and female-only samples,
ory test, and construction of the dependent variable), should not have been investigated at all. Rather the
these studies cannot provide solid insights into sex issue is that the hypothesis arguably remains to be put
differences since there may be methodological reasons to fully rigorous testing and so, despite the costs of
for different findings. A fifth study provided only false-positive errors, the confidence with which it is
within-group analyses which, as noted earlier, also presented by some experts seems premature.
do not enable statements about between-sex differen-
ces to be made [55]. Care in Citations of Potentially Spurious Results
The last two studies provided direct statistical tests of
sex differences in laterality of amygdala modulation of Once a reported sex difference is in the published
emotional memory [49, 57], but the dependent variable literature, the manner in which it is cited reflects the
used to compare laterality in the sexes was constructed extent to which the scientific community is sensitive
differently in the two studies (although the analysis of to the possibility of false-positive results. Two basic
[49] was repeated on [57], see last column of Table 2). ways in which scientists can demonstrate carefulness
This is not surprising since it is currently unclear how in their treatment of findings of sex differences are to
lateralization should be assessed [12]. However, the lack acknowledge any similarities also observed, and to
of established techniques increases researcher degrees take care to cite larger studies or meta-analyses that
of freedom [see 45], and it has been found that different failed to demonstrate a particular sex difference in
techniques and thresholds for testing laterality differ- favour of (or at the very least as well as) smaller
ences can yield markedly different results [12, 60]. studies with positive findings. Recent (2009 and
The final point to be made concerns sample sizes. 2010) citations of Shaywitz et al. [41] were chosen
The largest sample (24 participants in total) introduced to investigate this, by assessing how many noted the
Table 2 Studies presented in support of a sex difference in the modulation of memory consolidation by the amygdala for emotionally salient material
376

Study PET/fMRI Males Females Stimuli Memory test/delay Reported correlations between
amygdala activity and delayed
enhanced emotional memory
measures

Cahill et al. (1996) PET 8 0 Emotional (-ve) vs neutral Recall at 3 weeks Positive correlation found between
films right amygdala activity and number
of emotional (but not neutral) films
recalled.
Hamann et al. (1999) PET 10 0 Emotional (+ve and -ve) Recall and recognition at No findings for recall (possibly due
versus control (neutral 4 weeks to restricted range). Positive
and interesting) pictures correlations found between
bilateral amygdala activity and
recognition memory enhancement
for both positive and negative
pictures. For negative pictures,
this was described as “more
right-lateralized”, although no
statistical comparisons were
presented.
Canli et al. (1999) fMRI 0 10 Positive and negative Recognition memory Left amygdala activity correlated
pictures 2–14 months later with both positive and negative
recognition memory, right
amygdala activity correlated with
only negative recognition
memory.
Canli et al. (2000) fMRI 0 10 Negative and neutral Recognition memory at Positive correlation between left
pictures 3 weeks amygdala activation and
recognition memory for pictures
rated as highly emotional. Data for
other trials not included in the
analysis.
Cahill et al. (2001) PET 11 11 Emotional (-ve) versus Recall at 3 weeks Within-group conjunction analyses
8 previously reported in neutral films identified regions showing
Cahill et al. (1996) increased activity for emotional
compared with neutral films that
correlated with enhanced
emotional memory. In men, the
right amygdala was identified. In
women, the left amygdala activity
was identified.
C. Fine
Table 2 (continued)

Study PET/fMRI Males Females Stimuli Memory test/delay Reported correlations between
amygdala activity and delayed
enhanced emotional memory
measures

Canli et al. (2002) fMRI 12 12 Negative and neutral Recognition memory at Analyses were performed for highly
10 previously reported in pictures 3 weeks emotionally arousing pictures only.
Canli et al. (2000) Within-group analyses found a
positive correlation between right
amygdala activity and recognition
memory in men, and between left
amygdala activity and memory in
women. The significance levels of
the correlations were then used to
construct a “laterality index”
Is there Neurosexism in Functional Neuroimaging?

based on maximal amygdala


activity-memory correlations, used
to statistically test for the effects
of sex on laterality. This found a
significant group difference.
Cahill et al. (2004) fMRI 8 7 Negative and neutral Recognition memory at Within-group conjunction analysis
pictures 2 weeks identified regions where greater
activity was associated with both
better memory performance and
increasing arousal ratings. In men,
the right amygdala was identified.
In females, the left amygdala was
identified. Between-sex laterality
compared by using β representing
the modulation of memory by
arousal for the voxel of maximal
activation in the amygdala and β
for activation in the homotopic
voxel of the opposite hemisphere
as the dependent variables in a
sex-by-hemisphere ANOVA. The
significant sex x hemisphere
interaction was ‘replicated’ using
data from Canli et al. 2002.
377
378 C. Fine

sex similarities in brain activity observed for semantic Each citation was then categorized according to
and orthographic processing and how many also noted whether, and how, it referenced the existence of con-
the existence of contradictory evidence. This study tradictory findings (see Table 3 and Fig. 2). Forty-
was chosen due to the considerable counter-evidence three of the seventy-five (57 %) cited the Shaywitz
to the positive Shaywitz finding including the pub- study without referring to the existence of any contra-
lication of two meta-analyses [43, 44], and the time dictory data. Of the remaining 21 citations, eleven
period was one for which (at time of analysis) (15 % of the total) either failed to cite Sommer and
citing authors would have had the greatest opportu- colleagues’ work or did so in a way that was mislead-
nity to become apprised of those meta-analyses and ing, for example, describing the findings as showing
the data included in them. The Medline, Web of more bilateral activation in women [65]. A further
Science and PsycINFO databases were searched for nine studies cited one or both meta-analyses, but in a
all citations of the Shaywitz paper in 2009 and way that gave no indication that, through virtue of its
2010, and these were assessed to see how many status as a meta-analytic study, it lay claim to being a
researchers citing that study: first, did so in a way more reliable source of information than Shaywitz et
that acknowledged the absence of sex differences in al. Thus, just twelve of the 74 (16 %) studies that cited
brain activation for two of the three language tasks; the Shaywitz finding also cited the work of Sommer
and second, acknowledged subsequent null findings and colleagues in a fully informative way (even if the
(see Table 3 and Appendix for details). latter’s conclusions were disputed).
There were 92 citations of the article during the
2 year time period. Non-English language articles
were excluded from the sample (n04), as were cita- Exaggeration of Functional Significance
tions that were erroneous (e.g., relating to the comor- of Male/Female Brain Activation Differences?
bidity of language disorders and ADHD), inaccurate Functional Obscurity
or vague (e.g., misrepresenting the finding as being in
a non-language domain, or as providing a possible A second major difficulty for neuroscientists is to con-
neurobiological explanation for greater numbers of duct research in ways that can yield understanding of the
boys having reading difficulties), or that referenced functional implications, if any, of sex differences in
the findings of the article in a non-gender-specific brain activation [see 10]. FNI can be used to make
way (n012). In addition, a book chapter by Sommer ‘forward inferences’ about which regions of the brain
(2010) was excluded for obvious reasons. Citations are candidates for involvement in a particular psycho-
that referred to the findings as being in the wrong logical process. Sex comparisons can then further estab-
language domain (e.g., “listening to speech”) or in a lish whether and how these neural correlates differ
non-specific way (e.g., “high-level cognitive process- between the sexes. Making further inferences about
ing”) were included. This resulted in a sample of 75 mental processes from differences in neural activity
citations of the Shaywitz study as demonstrating a between experimental and control conditions requires
neurological sex difference in brain activation either making ‘reverse inferences’; that is, claims of the form
during language processing or in processing in gener- ‘Brain Region X showed increased activation therefore
al. Of these 75 citations, only three referred explicitly Mental State Y was present.’ However, mental process-
to the absence of findings of sex differences in brain es arise from the complex and dynamic interaction of
activity for orthographic and semantic processing multiple brain regions that themselves comprise a stag-
within the Shaywitz study itself [12, 42, 64],3 al- gering complexity of connections. Conversely, any par-
though several other citations noted more generally ticular population of neurons will be recruited by
that lateralization differences applied specifically to multiple mental processes [see 66]. The absence of neat
phonological processing. one-to-one mapping between brain regions and mental
processes renders reverse inferences logically invalid
3
(although the probability that brain activity in region X
It’s noteworthy (or at least footnoteworthy) that two of these
indicates the presence of mental state Y increases to the
three articles are specifically concerned with problems arising
from neuroimaging studies of sex differences in language extent that X is exclusively activated by Y [67, 68]).
lateralization. Also, not only can activity be linked only extremely
Is there Neurosexism in Functional Neuroimaging? 379

Table 3 Studies citing Shaywitz et al. (1995) in 2009 and 2010, categorized according to the extent to which contradictory data are also
cited, including two meta-analyses

Context in which Shaywitz et al. (1995) is cited Studies (by first author)

Excluded: incorrect/inaccurate/non-gender specific Binder, Boyd, Chen, Gillies, Hansen, Hazlett, Limbrick, Locascio,
citations (n012)a Maruyama, Merz, Ohuchida, Stevens-Smith
No contradictory data cited (n043) Allez, Badcock, Blakemore, Breier, Brugger, Byrnes, Caparelli, Capone,
Costafreda (a), Cousin, Draca, Feinstein, Fink, Ford, Galambos, Gorbet,
Hartwigsen, Henderson, Hines, Hockenbury, Isman, Iwabuchi, Jahanshad,
James, Kempe, Lenroot, Lopes, Lv, Majovski, Sereno, Sousa, Sternadori,
Strong, Tong, Tranel, Van Dyke, Van Strien, de Vries, Van Wormer, Weis,
Wheldall, Wilde, Yousem
Contradictory data cited
No citation of Sommer/Sommer cited incorrectly (n011) Cahill*, Darlington, Gauthier, Kivilevitch, Li, Logan*, Lyttelton, Rumberg,
Semrud-Clikeman, Jancke, Mbwana
Sommer as if of equivalent warrant (n09) Bitan, Costafreda (b), Geary, Gordon, Hausmann, Lebel, Liu, Sava, Reiterer
Sommer cited as holding greater warrant (n012) Andreano, Chiarello, Cowell, Garn, Ihnen, Kaiser, Kherif, McManus,
Pinel, Stelnikov, Wallentin, Zaehle
a
Also excluded were four non-English articles and a book chapter by Iris Sommer (see main text)
Asterisked (*) studies cite a critical review paper [37]

speculatively with a particular mental process, but cor- activity associated with a psychological function com-
relation does not demonstrate causation. A number of pared with a control task, the psychological meaning
studies have shown significant activity in regions that, of which is even more obscure than the difference
from other techniques, appear not to be crucially in- itself. For example, a sex difference in brain activity
volved in task performance [e.g., 69, 70]. Moreover, could reflect a difference in either degree of activation
greater activation doesn’t imply ‘more’ mental process, of the same neural circuitry, or the use of different
since development or practice can lead to ‘streamlining’ neural circuitry to perform the same task. It is also
of neural activation [71–73]. possible that sex differences in brain activity have no
How, then, to interpret sex differences in brain functional significance, and merely reflect a different
activity in a particular region? As Bluhm [15] has neural means to the same behavioral ends [31]. The
noted, researchers interested in sex differences have danger to researchers is that gender stereotypes can be
to interpret “a difference in a difference” in the brain readily drawn upon to interpret these highly ambigu-
ous data. For example, it has been noted [10] that the
No contradictory absence of empirical or theoretical grounding for spec-
data ulations about brain-mind relations in visuo-spatial
16% processing means that precisely opposite hypotheses
can be equally plausible [74], and that hypotheses can
No (or incorrect) be revised post hoc in ways that maintain the over-
12% Sommer citation riding assumption that the male brain is superior [75,
76]. Bluhm [14] has likewise documented how three
57%
studies respectively showing greater [77], lesser [78],
15% Sommer cited as and similar [79] activity in the male prefrontal cortex
equivalent warrant were all interpreted as suggesting greater cognitive
control of emotion in males, in line with a long-
standing gender stereotype.
Fully informative Poldrack [68] has argued that reverse inferences are
Sommer citation a useful research tool when used to generate hypoth-
Fig. 2 Studies citing Shaywitz et al. (1995) in 2009 and 2010, eses to put to test in further empirical work. Thus
categorized according to citation of contradictory data while there is certainly arguably a place for post hoc
380 C. Fine

speculation based on exploratory research, it should the studies were exploratory. A further eight studies
form part of a larger strategy of the systematic devel- were categorised as ‘empirically-derived-vague’, and
opment and testing of predictions derived from in- the remaining twenty-three were categorised as
creasingly well-specified neurocognitive accounts of empirically-derived-precise. No study was categorised
the sex-modulated processes involved in the behavior as ‘hypothesis-driven.’
under investigation. This would reduce the scope for Second, studies were examined for the presence of
false-positive errors, as well as the scope for untested reverse inferences in interpretation of findings: that is,
stereotype-infused speculations about the functional speculations about the psychological meaning of ob-
significance of neurological findings. The importance served sex differences in brain activity. If reverse
of such an empirically and theoretically grounded inferences were made, it was noted first whether any
approach was recently stressed by Park and Huang relevant behavioral data were available. If so, it was
[80] in their discussion of the perils of investigating then noted whether those data were consistent or in-
cultural influences on the brain, noting that it is “crit- consistent with the reverse inference. Twenty-seven of
ical that specific hypotheses grounded in knowledge the 39 studies (69 %) suggested reverse inferences,
of neural structures and behavioral data be tested. … speculating either a quantitative difference in male/
[This enables us] to test specific hypotheses in regions female responsiveness to the experimental stimuli
of interest and limit the amount of neural “real estate” (e.g., “greater, more widespread activation may sug-
under investigation, increasing the prospects of find- gest that males recruit less expert neural systems when
ing interpretable, replicable differences that are related processing emotional stimuli” [81, p. 143]), and/or a
to cultural values and beliefs [rather than other factors qualitative difference in mental processing (e.g., the
not of interest].” “pattern of findings is consistent with the higher emo-
To what extent, then, does recent FNI research on tional reactivity and emotion-focused coping style com-
sex differences, through the use of research driven by monly observed among females … [observed male
well-specified neurocognitive models, constrain the neural activity] is probably related to the cognitive effort
potential for neurosexist speculations? This question and specific regulatory strategies that they had
was investigated with the set of thirty-nine 2009 and employed.” [82, p. 2907]). Behavioral data relevant to
2010 fMRI studies described previously (see Table 4). the reverse inference (e.g., performance data if greater
First, studies were examined for the presence or ab- male/female expertise was speculated from brain acti-
sence of a prediction regarding expected sex differ- vation differences, or behavioral measures of strategy
ences in brain activity. Studies categorised as differences if those were inferred) were available in 14
‘exploratory’ presented no such predictions. Studies of the 29 studies in which reverse inferences were made.
categorised as ‘empirically-driven-vague’ made im- Strikingly, however, in 11 of these 14 studies the
precise predictions of the brain regions in which they relevant available behavioral data were inconsistent
expected sex differences to be observed, based on with, or unsupportive of, a reverse inference made
previous empirical findings. Studies categorised as (see last column of Table 4). For example, Klucken
‘empirically-driven-precise’ made more precise pre- et al. [83] looked at brain responses to conditioned
dictions of this kind. A liberal definition was used, in sexual stimuli, and found greater neural response in
which even very broad-brush predictions of differen- males in the amygdala, brainstem, thalamus and oc-
ces in large regions of the brain (e.g., “parietal lobe”) cipital cortex. They suggested that these neural differ-
were categorised as precise, so long as the direction of ences reflect the greater capacity of men to be
difference was specified. Studies categorised as ‘hy- conditioned for sexual arousal. However, their behav-
pothesis-driven’ drew on neurocognitive models to ioral data contradicted this suggestion. Despite the fact
make precise predictions of the brain regions in that the female participants found the unconditioned
which they expected sex differences to be observed, stimuli (erotic pictures) less positive and sexually
corresponding to specific mental processes thought to arousing than did men, they nonetheless rated the
differ between the sexes. Where a study included sexually conditioned stimuli similarly to men on
predictions of more than one type (e.g., both ‘vague’ arousal, valence and sexual arousal. If anything, this
and ‘precise’ empirically-derived predictions), they indicates a greater female capacity for sexual condi-
were placed in the more precise category. Eight of tioning. Similarly, Lee and colleagues speculated that
Table 4 Predictions, reverse inferences and consistency with available behavioral data for 2009 and 2010 fMRI studies of sex differences

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Aikins Sex-related differences in Empirically-based-vague: Suggest that increased amygdala False positive rates Inconsistent in that false
amygdala activity influences “examined whether the activation increases long-term measured. No measures of positive rates did not differ
immediate memory [predicted] relationship retention of arousing material semantic encoding. between the sexes at the
between lateralized amygdala in men, but produces increased group level.
activation and false-positive coherence in unpleasant pic-
rate differed as a function of tures in women due to semantic
participant sex” (273). encoding, that may result in
difficulty discriminating be-
tween unpleasant pictures in
women.
Bitan Bidirectional connectivity Exploratory. Notably, findings – – –
between hemispheres occurs are directly contradictory with
Is there Neurosexism in Functional Neuroimaging?

at multiple levels in language standard accounts of the


processing but depends on sex functional effects of sex
differences in language
lateralization.
Christakou Sex-dependent age modulation Empirically-driven-vague: “we “the superior reliance on functional No measures of –
of fronto-striatal and hypothesised that gender frontal mechanisms in females, hypothesised strategy
temporo-parietal activation would affect prefrontal, striatal and on functional parietal differences (e.g., visual-
during cognitive control and parietal brain activation, mechanisms in males may spatial strategies in males
as well as the age modulation underlie aspects of the well- versus top-down inhibi-
of these regions.” (224) documented differences in cog- tion strategies in females).
nitive strategies and relative abil-
ities between the sexes.” (234)
Clements-Stephens Developmental sex differences Empirically-driven-precise: The differences in activation No measures tapping –
in basic visuospatial “hypothesized that with patterns in females “could be strategies, no sex
processing: Differences in increasing age, males would mediated by a verbal strategy difference in performance
strategy use? develop a bilateral used early in development. on task, nor male
representation of visuospatial Additionally, differences seen advantage on other
processing in parietal regions in males are consistent with visuospatial tasks
shown by the utilization of right visually based strategy use in established for this
hemisphere regions in younger- which it is suggested that sample.
aged participants and the en- males rely on imagery and are
gagement of left hemisphere ‘more hands-on’ during task
regions later in adolescent completion. Moreover, males’
males. For females, we pre- reliance on a visuomotor net-
dicted that we would see a con- work could account for the
sistent right hemisphere network traditional advantage on
in frontal and parietal regions visuospatial tasks.” (160, all
regardless of age.” (156). references removed)
381
Table 4 (continued)
382

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Coman The effects of gender and Empirically-driven-vague: “we – – –


catechol O-methyltransferase hypothesize that COMT
(COMT) Val108/158Met genotype will have a sexually
polymorphism on emotion dimorphic effect on brain
regulation in velo-cardio- activation, especially in areas
facial syndrome (22q11.2 such as the amygdala and other
deletion syndrome): An limbic structures that have been
fMRI study previously shown to have
differential activation during
emotional processing in the
general population.” (1044)
Cornier Sex-based differences in the Empirically-based-vague: “women are more sensitive or Some loosely relevant Consistent. Women showed
behavioral and neuronal “hypothesized that women would ‘reactive’ to food-related cues measures. increased post-meal satiety
responses to food have a greater cognitive or frontal than men … have greater at- ratings, and were more
response to food-related visual tention (parietal response) and likely to maintain isocaloric
stimuli than men which would be cognitive processing (prefron- intake during ad libitum
related to the behavioral meas- tal response) related to food feeding, which was corre-
ures [greater sensitivity to hunger stimuli. The greater DLPFC lated with DLPFC response
and satiety responses, resulting in activation in women may also to visual food cues.
greater capacity to maintain en- suggest a greater inhibitory re-
ergy balance].” (539) sponse to the food cues.” (542)
Derntl Multidimensional assessment Empirically-based-precise: “we Emotion recognition: “females No measures of ‘emotional’
of empathic abilities: Neural assume that during emotional rely on autobiographical versus ‘cognitive’
correlates and gender perspective taking and memory to correctly label the strategies to the various
differences emotion recognition females emotional expressions.” (77) tasks. No measures of
will recruit more emotion- Emotional perspective-taking: tendency to share
related regions such as the in- “males might rely more strongly emotions with others.
ferior frontal and superior on a perceptual-analyzing net-
temporal gyrus, while males work and mentalizing abilities
will exhibit stronger activation than do females who rather re-
in the temporo-parietal junc- cruit regions associated with
tion. Finally, for affective re- emotional contagion and affec-
sponsiveness we hypothesize tive responsiveness when
overall stronger neural activa- assessing the emotional expres-
tion in female subjects, and sion of another person support-
particularly in the superior ing the view that men probably
temporal and medial-frontal have a lower tendency to share
regions as well as the their emotions with others than
amygdala.” females.” (77–8, reference
removed)
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

“we also conducted exploratory Affective responsiveness:


analyses concerning the “females relied more on
influence of cycle phase on the emotional regions to
activation pattern and experience the emotion, while
suggested more pronounced males show a different neural
responses in emotional strategy … supporting
networks during the follicular assumptions of a more
phase.” (69) cognitive route.” (78)
Empathy network: While females
recruited regions “associated
with emotion imitation and
evaluation, males rather relied
Is there Neurosexism in Functional Neuroimaging?

on a region known to be
involved in semantic retrieval
… thus indicating a rather
cognitive approach.” (79)
“we also observed a strong trend No behavioral sex Inconsistent. No performance
towards a significant general differences observed on differences between women
task independent impact of any task (other than self- in different menstrual
menstrual cycle phase on report). phases.
amygdala activation further
supporting the assumption
that the hormone status during
the follicular phase facilitates
sensitivity and behavior in
socio-emotional-situations.
This may be traced back to the
evolutionary advantage of
higher attention and respon-
siveness to social-emotional
interactions thereby improv-
ing mating chances during
times of increased fertility.”
(78, references removed)
Domes The neural correlates of sex Empirically-derived-precise: “the recruitment of prefrontal areas Post-scan valence and Inconsistent. No sex
differences in emotional “We hypothesized that women during the initial processing [in arousal ratings of stimuli differences in post-scan va-
reactivity and emotion show enhanced initial women] might reflect effortful measured, as well as lence and arousal ratings of
regulation emotional responding to cognitive processing, such as the subclinical symptoms of stimuli. No sex differences
aversive stimuli compared to allocation of attentional resources depression and trait
383
Table 4 (continued)
384

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

men, associated with enhanced to the emotional aspects of the anxiety. No measures of on subclinical symptoms of
activity in emotionally stimulus, which have been emotional response post- depression and trait anxiety.
relevant brain areas, in enhanced in women compared to regulation taken. No
particular the amygdala. In men. Alternatively, women measures of attention to
addition, women were might have attempted to decrease emotional stimuli or ag-
expected to show attenuated their emotions as soon as the gressive tendencies taken.
activity in the areas subserving aversive stimuli appeared.
the cognitive regulation of However, as women showed
emotional responses, namely enhanced amygdala responding
in the dlPFC, OFC, and ACC in the initial viewing phase, these
when attempting to decrease attempts might have been less
their initial emotional effective compared to men.”
reactions to negative stimuli.” (767)
(760) “our data in part support the idea
that women may be more
vulnerable to depression
because they tend to be more
reactive to emotional stimuli and
are less effective in regulating
their emotional response.” (767)
“increased amygdala activity to
negative stimuli in men during
cognitively increasing
emotional responses might
also have implications for the
neural basis of maladaptive
behaviors associated with
enhanced emotional
responding to aversive
interpersonal stimuli that is
more prevalent in men, e.g.,
aggressive behavior. The
present results suggest that
emotionally laden aggressive
behavior might not only be
due to difficulties in impulse
control, but might also be
promoted by the relative ease
of voluntary emotional up-
regulation in men.” (767)
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Eisenberger An fMRI study of cytokine- Exploratory – – –


induced depressed mood and
social pain: The role of sex
differences
Elsabagh A longer duration of Empirically-based-precise: – – –
schizophrenic illness has “hypothesised that a longer
sex-specific associations illness duration would be
within the working memory associated with decreased
neural network in activation of the PFC during
schizophrenia performance of a WM task
and may be accompanied by
compensatory effects in other
Is there Neurosexism in Functional Neuroimaging?

brain regions. Furthermore,


we hypothesized that these
effects would be more
pronounced in male patients
than in female patients.”
(42)
Felmingham Neural responses to masked Empirically-based-precise: “greater brainstem activation to No measures of arousal or –
fear faces: Sex differences “predicted that (a) trauma- fear may contribute to the orienting to threat, or
and trauma exposure in exposed women would have greater prevalence of PTSD in capacity to contextualise
posttraumatic stress disorder greater activity in fear and women [through heightened fear-related stimuli
arousal networks than would arousal and orienting to
non-trauma-exposed women, threat], greater hippocampal
trauma-exposed men, and activation in men may
non-trauma-exposed men; subserve an enhanced capacity
(b) both PTSD men and for contextualizing fear-
women would display great- related stimuli.” (246).
er fear and arousal network
activation than trauma-
exposed and non-trauma-
exposed women and men;
(c) women with PTSD
would display greater activi-
ty in fear networks than
would PTSD men.” (242)
Fine Gender differences in BOLD Empirically-based-precise: Two “plausible” inferences are No behavioral measures –
activation to face “hypothesized greater right that “the males in our study taken
photographs and video lateralization in males interpreted the stimuli
vignettes compared to females to photos differently than did the
385
Table 4 (continued)
386

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

in the social network formed females” or “that males are


by the amygdala, frontal gyri actually less efficient at
and anterior cingulate. … processing the stimuli …
hypothesized gender greater, more widespread
differences in the right and left activation may suggest that
temporal regions that process males recruit less expert
the various aspects of neural systems when
language [specifically greater processing emotional stimuli.”
left lateralization in males].” (143). Also speculate that
(138) “male responses included ad-
ditional checking to be sure
that the positive stimuli were
genuine and without threat at
the preconscious level”, in
reference to supposed greater
male responsiveness to threat-
ening stimuli (143–4)
Frank Processing of food pictures: Exploratory “higher [superior medial No measures of self –
Influence of hunger, gender frontal lobe] activation in perception concerning
and calorie content women while viewing high- food.
caloric pictures when hun-
gry compared to being not
hungry. … These might be
related to different self per-
ception of men and women
concerning food processing”.
(164)
Garn An fMRI study of sex Empirically-driven-vague: that Suggest that activation No behavioral measures –
differences in brain “men and women might differ differences may be due to taken (silent naming task).
activation during object in terms of hemispheric differential lexical selection
naming processing distribution during versus retrieval demands for
object naming” (611) and that men versus women, stemming
there may be sex differences in from sex differences in
regions related to either choice vocabulary size.
selection or word retrieval,
corresponding to contrasting
hypotheses about the reason
for behavioral sex differences
in naming living versus non-
living objects.
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Gauthier Sex and performance level Empirically-based-vague: “men seem to make greater use No measures of strategy –
effects on brain activation “The aim of this study was to of visual mental strategies … taken.
during a verbal fluency task: test whether (1) difference in than the usual phonological
A functional magnetic neural correlates between and semantic strategies”
resonance imaging study sexes exist in a covert fluen- (175).
cy task, irrespective of high
or low level performance, (2)
performance differences are
related to neural activity re-
gardless of sex for this same
task and (3) sex and levels of
performance act in an addi-
Is there Neurosexism in Functional Neuroimaging?

tive or interactive manner on


neural area activation … our
attention was drawn to un-
derstanding (4) whether the
precuneus, occipital gyri and
cerebellum would be differ-
entially engaged to resolve
the task according to perfor-
mance and/or sex factors”
(165).
Goldstein Sex differences in stress Empirically-based-precise: “From an evolutionary point of No measures of judgment of Inconsistent. No group
response circuitry activation “predicted that men would view, it is important for the threat level of relevant differences in mood or
dependent on female look more similar to women in female during midcycle to stimuli taken. anxiety measures before or
hormonal cycle [early follicular] than during have a heightened cortical after viewing aversive
[late follicular/midcycle capacity, unencumbered by images. See main text for
phase], given the greater excessive arousal, to further discussion.
similarity of men’s hormonal optimally judge whether a
status to women’s hormonal potentially threatening
status at [early follicular] stimulus, such as an
compared to [late follicular/ approaching male, is an
midcycle phase].” (432). opportunity for successful
mating or for fight or flight.
Thus, females have been
endowed with a natural
hormonal capacity to
regulate the stress response
that differs from males.”
(437)
387
Table 4 (continued)
388

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Ino Gender differences in brain Exploratory “the reduced activation observed Facial recognition Inconsistent. No sex
activation during encoding in women compared to men performance measured. differences in performance
and recognition of male and during encoding suggests that (although this is attributed
female faces the relevant cerebral regions to a ceiling effect).
were recruited more efficiently
in women. Therefore, this
fMRI finding provides the
neuronal basis for the
superiority of women over men
regarding facial recognition,
which has been indicated by
previously behavioral studies
but was not duplicated in the
present study, probably due to
the ceiling effect.” (2)
Keller Gender differences in the Empirically-based-precise: “we – – –
functional and structural predicted that … (2) gender
neuroanatomy of differences in brain responses
mathematical cognition would exist even in the absence
of overt gender differences in
behavior, (3) males and females
would show extensive overlap
in activation of the left and right
IPS and angular gyrus … and
(4) males would show greater
activation in the PPC whereas
females would show greater
responses in the left and right
frontal cortex.” (343)
Kempton The effects of gender and Empirically-based-precise: “that Findings suggest that No relevant behavioral –
COMT Val158Met females homozygotes for the “emotional mimicry is measures taken.
polymorphism on fearful Met allele, would … show perhaps minimal in males
facial affect recognition: a amplified task-induced activa- whereas in females there may
fMRI study tions within limbic regions … be increased inhibition in this
possible that a genotype- region” (377).
associated prefrontal-
associated mechanism can
override the effect of the
genotype within the limbic
regions.” (372)
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Killgore Sex differences in cerebral Empirically-based-precise: “Though speculative, [greater Self-reported appetite and Inconsistent. No sex
responses to images of high “hypothesized that females activation patterns in control of eating behavior differences in self-reported
versus low-calorie food would show greater overall particular regions in women in measured. No other appetite or control of eating
activation in response to high- response to calorie-rich food] relevant behavioral behavior.
calorie food images, particu- may reflect increased engage- measures taken.
larly within prefrontal inhibi- ment of prefrontal evaluative,
tory and self-monitoring decision-making, inhibitory,
regions compared with males. and self-referential cognitive
Furthermore … it was hy- systems” (357). Other sex
pothesized that women would differences in activation
show greater activation than “reinforces the notion that
men within [the insula and women may process food im-
Is there Neurosexism in Functional Neuroimaging?

amygdala].” (354) agery at a more complex cog-


nitive/somatic level, whereas
men may process food stimuli
at a less complex hedonic
approach-withdrawal level.”
(358)
Klucken Neural activations of the Empirically-based-vague: Results “in line with current Subjective sexual arousal Inconsistent. No sex
acquisition of conditioned “hypothesized that … men findings suggesting that men ratings of conditioned differences in subjective
sexual arousal: Effects of would show increased are more receptive to stimuli measured, as well arousal ratings of
contingency awareness and responses” to conditioned conditioning of sexual arousal as skin conductance conditioned stimuli. (No
sex stimuli relative to neutral stimuli, than women” (3081), responses (SCRs). effect of conditioning on
compared with women (3072). SCRs.)
Krach Are women better Empirically-based-precise: “we – – –
mindreaders? Sex differences expected … that women
in neural correlates of would be better perspective
mentalizing detected with takers and therefore display
functional MRI stronger signal changes in the
medial prefrontal cortex.” (2)
Lee Sex-related differences in Empirically-based-precise: “Our findings regarding the No relevant behavioral Inconsistent. No sex differences
neural activity during risk “hypothesized that the male and stronger activation in the OFC measures other than risk- in either rate of making risky
taking: An fMRI study female participants would show for the female participants taking itself. responses, or response time to
differential patterns of neural than for the male participants make risky responses.
activation associated with risk suggests that women need to
taking. … that when the female partake in a higher degree of
and male participants showed mental consideration before
comparable rates of risky making a risky response.”
selection, the neural activations (1308)
in the insula and the OFC
389
Table 4 (continued)
390

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

would be stronger for the Greater “responsiveness [in


female participants than for the particular brain regions in
male participants. … We females] may arise because
hypothesized that stronger the female participants are
correlations [between right more mentally alert than the
insula and the OFC with the rate male participants when
of risky selection and updating and valuating their
punishment] would be obtained subsequent actions during the
for the female participants than task.” (1308)
for the male participants.” “it is likely that the male
(1304) participants, relative to their
female counterparts, were more
active in encoding the positive
experience from the reward
feedback. The encoded positive
experience may render men
than women more ready for
committing to subsequent risk-
taking behaviors.” (1310)
“The stronger OFC and insula
activities in women than in
men may reflect the sensitivity
of women to situations of
ambiguity … [This] could
make women more risk averse
than men.” (1310).
Li Gender differences in Exploratory “These opposite patterns of No relevant behavioral –
cognitive control: An cerebral responses between [stop measures taken, and no
extended investigation of the success] and [stop error] trials behavioral differences on
stop signal task suggested there were perhaps the task.
fundamental differences in the
way men and women perform
the stop signal task.” (270).
“This [neurological] gender
difference … along with
greater error-related activity in
women, as compared to men,
may indicate fundamental dif-
ferences in the temporal
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

dynamics with which men and


women respond to errors dur-
ing a cognitive task that
requires moment-to-moment
monitoring of performance.”
(270)
“PCC activity may also reflect
that, compared to men,
women were involved to a
greater extent in ‘mental
reflection’” (270).
Is there Neurosexism in Functional Neuroimaging?

Mak Sex-related differences in Empirically-based-precise: “we The “pattern of findings is Self-reported regulatory Consistent. Marginally
neural activity during hypothesized that during consistent with the higher strategies measured. significant (p0.066) trend
emotion regulation emotion regulation, males emotional reactivity and for females to report more
would mainly recruit the emotion-focused coping style emotion-focused regulatory
dorsolateral prefrontal regions commonly observed among strategies and males to re-
that are implicated in cognitive females. … [Observed male port more cognitive-
processes, while females would activity] is probably related to focused strategies.
mainly recruit the orbitofrontal the cognitive effort and spe-
regions that are implicated in cific regulatory strategies that
affective processes.” (2901). they had employed.” (2907).
Mather Sex differences in how stress Empirically-based-precise: “for “it seems that coordination of No relevant behavioral –
affects brain activity during men observing other’s emotions, basic face processing by the measures taken, such as
face viewing stress will decrease interactions FFA and interpretation and tendency to social
between the amygdala and brain simulation of emotional affiliation in response to
regions such as the insula and expressions by the extended stress.
temporal pole that help people temporal pole region
understand others’ state of mind increased under stress for
and simulate others’ emotions, women but decreased for men.
whereas for women, stress will This pattern is consistent with
increase interactions among behavioral findings that stress
these regions. In addition, it is promotes social affiliation for
hypothesized that, for men, women but disrupts it for
stress will decrease coordination men.” (936, reference
between a brain region engaged removed)
in basic visual processing of
faces (the fusiform face area or
FFA) and regions engaged in
simulating and interpreting
391
Table 4 (continued)
392

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

facial emotions (the temporal


pole and insula) whereas, for
women, stress will increase
coordinated activities among
these regions.” (933, references
removed)
Merz Investigating the impact of sex Empirically-based-precise: “Women were more prone to a SCRs measured. Consistent. Cortisol
and cortisol on implicit fear “predicted that cortisol would facilitation of [the insula] during enhanced mean SCR to the
conditioning with fMRI reduce the CS+/CS- enhanced [glucocorticoid] levels conditioned stimulus in
differentiation in men, while possibly revealing an women but reduced it in
enhancing them in women in unconscious shift towards the men.
[the amygdala, the acquisition of potential danger
hippocampus, or the thalamus] cues in a stressful situation.”
and additionally in the frontal (42)
cortex.” (35)
Ohrmann Effect of gender on processing Empirically-based-precise: “strongest amygdala activation No threat judgment –
threat-related stimuli in “postulated a stronger in women was observed after measures taken.
patients with panic disorder: activation of the neural fear exposure to angry and neutral
Sex does matter circuitry in response to threat- faces, implying that these two
related stimuli in female [panic facial expressions are the most
disorder] patients, as com- threatening to women.”
pared to the male patient (1041)
group.” (1035)
Owens An fMRI study of self- Empirically-based-precise: that “when females [but not males] Measures of body image Inconsistent. Both sexes
reflection about body image: “females might show stronger are confronted with fat images concern and post- scored extremely low on a
Sex differences activation in mPFC when and asked to apply this criterion experiment reports of self- measure of body image
engaged in self-reflection to their own bodies, they are reflection taken. concern.
about their bodies” (850). more inclined to seriously
engage processes of self-
reflection and (re)evaluate rel-
evant self-representations given
the cultural directive of thin-
ness for female bodies.” (853)
“results provide converging
evidence of a stronger
relationship between body
size and self-representation for
women than for men and they
provide further support for the
hypothesis of a number of
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

theorists that a typical, non


eating disordered woman in
US society shows a relatively
high level of concern for body
shape.” (853)
Qiu The effects of acupuncture on Empirically-based-vague: “we – – –
the brain networks for hypothesize that women and
emotion and cognition: An men may have different brain
observation of gender activation/deactivation
differences patterns at the [limbic–
paralimbic–neocortical
network] and the [default
Is there Neurosexism in Functional Neuroimaging?

mode network] in response to


acupuncture procedure.” (57)
Reidl Are there neural gender Empirically-based-precise: eight “Our fMRI data (i.e., the Perceived trustworthiness Inconsistent. Women gave
differences in online trust? specific hypotheses made. striatum activation) provide of offers measured, but no higher ratings of
An fMRI study on the empirical support that women behavioral measures of trustworthiness than men.
perceived trustworthiness of consider socio-psychological functional versus social/
eBay offers and emotional concerns most emotional motivations in
relevant in both conventional shopping, of emotional
shopping and online shop- versus cognitive
ping.” (416) processing, or of
Larger cluster size of dorsal perception of uncertainty
anterior cingulate cortex or risk.
activation in men “supports
the notion that men, in
contrast to women, usually
process information in a
cognitive rather than affective
manner” (417, references
removed).
Task “triggered activation in
more brain areas for females
than for males … This pattern
of female brain activation may
occur because women
perceive greater levels of
uncertainty and risk” (419,
reference removed).
393
Table 4 (continued)
394

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Rubia Effects of age and sex on Empirically-based-precise: “Males seem thus to have relied No behavioral measures of Inconsistent. Males and
developmental neural “expected to observe more on bottom-up parietal processing style females did not differ in
networks of visual-spatial at- enhanced frontal activation visual-spatial perception differences. Mean mean reaction time on
tention allocation in females and enhanced mechanisms for stimulus sa- reaction time and error either congruent or oddball
parietal activation in males liency processing, while rates measured. trials, although the increase
during visuospatial attention females appear to have relied in reaction time on oddball
allocation. Furthermore, … more on top-down fronto- trials compared to
we hypothesised that brain striato-temporal executive congruent trials was greater
regions that differed in control of selective attention, for females than for males.
activation between males and which may be slower and less
females would be related to effective than more automatic
underlying sex differences bottom-up processes used by
in the neurofunctional males.” (824).
maturation of these brain
regions, with more
pronounced maturation of
parietal regions in males and
frontal regions in females.”
(818).
Rumberg Cycle and gender-specific ce- Empirically-based-precise: – – –
rebral activation during a “hypothesize that the
verb generation task using lateralization of the activation
fMRI: Comparison of wom- patterns will differ in women
en in different cycle phases, dependent on their hormonal
under oral contraception, and status, leading to significant
men activation in the frontal and/or
temporal areas for women
under oral contraception
compared to women without
oral contraception in two
different cycle phases.
Concerning the gender
differences, we assume that
the previously described
differences between men and
women in the temporal cortex
[higher in males] will be
verified, but hypothesize that
this finding will also depend
on the cycle time.” (367).
C. Fine
Table 4 (continued)

Study (by first Title Prediction Reverse inference Relevant behavioral data Behavioral data consistent
author) available? with reverse inference?

Schmidt No gender differences in brain Empirically-based-precise: – – –


activation during the N-back “initial tentative hypothesis
task: An fMRI study in was that men would show
healthy individuals greater activation in frontal
and parietal regions than
women [in a verbal working
memory task].” (3610)
Straube Sex differences in brain Exploratory “On the basis of the putative No relevant behavioral –
activation to anticipated and role of the anterior MPFC, measures taken.
experienced pain in the increased activation in this
medial prefrontal cortex area [in females] suggests
stronger self-related process-
Is there Neurosexism in Functional Neuroimaging?

ing of anticipated and experi-


enced, clearly painful stimuli
in women, as compared to
men.” (697).
Sveljo Gender differences in brain Exploratory “Our results may suggest that No behavioral measures –
areas involved in silent gender related differences in taken. Silent counting
counting by means of fMRI language processing reflect task.
specific cognitive and
executive strategies as a
response to certain stimuli”
(7).
Valera Sex differences in the Empirically-based-precise: – – –
functional neuroanatomy of “predicted that … functional
working memory in adults differences [between adults
with ADHD with ADHD and comparison
subjects, including frontal
hypofunction and right frontal-
striatal-cerebellar abnormali-
ties] would be smaller for the
women with ADHD than for
the men” … “we also con-
ducted exploratory analyses to
assess the correlation between
ADHD symptoms and neural
activation associated with per-
formance on the working
memory task for men and
women separately.” (87)
395
396 C. Fine

observed male/female brain activation differences


Behavioral data consistent suggested that women “need to partake in a higher
with reverse inference? degree of mental consideration before making a
risky response, and render women more risk


averse” [84, p. 1308], even though they found no
sex differences in either response time to make, or
number of, risky responses. In both cases, it
appears that, in interpreting their highly ambiguous
neurological data, assumptions about likely sex dif-
Relevant behavioral data

ferences in behavior (in sexual conditionability and


taste for risk) had greater influence than the similarity
actually observed.

Other interesting examples of psychological spec-


available?

ulations unsupported by behavioral data were provid-


ed by two studies investigating hormonal influences
on female brain activity. Derntl et al. [85] looked at
brain activity during the performance of a number of
empathy tasks and found a non-significant trend for
greater amygdala activity in six women in the follicu-
lar phase of the menstrual cycle, compared with six
Reverse inference

women in the luteal phase. Given the role of the


amgydala in socio-emotional processing they sug-
gested that “the follicular phase facilitates sensitivity

and behavior in socio-emotional situations [references


removed]” and that this facilitation “may be traced
back to the evolutionary advantage of higher attention
related lateralization of amyg-

dependent in [emotional en-


hancement of memory]” (2)

and responsiveness to social-emotional interactions


Empirically-based-precise: to
“explore whether the sex-

thereby improving mating chances during times of


dala function is time-

increased fertility.” [85, p. 78]. However, no differ-


ences in empathizing ability were observed between
women in different phases of their cycle. A second
Growing together and growing Exploratory

study investigated the effect of menstrual cycle phase


Prediction

on brain responses to aversive stimuli [86]. The


authors reported greater attenuation of brain activity
in subcortical regions, including the amygdala, rela-
developmental trajectories of
enhancement-related effects
of emotional memory time-

tive to males, in twelve women when in the late


differences in the lifespan
amygdala to the sex- and

follicular/mid-cycle phase compared with the early


apart: Regional and sex
Is the contribution of the

functional homotopy

follicular phase. From this finding the authors sug-


gested that hormonal changes in women may influ-
ence stress responses such that the mid-cycle female
dependent?

can “optimally judge whether a potentially threaten-


ing stimulus, such as an approaching male, is an
Title

opportunity for successful mating or for fight or


Table 4 (continued)

flight.”[86, p. 437] However, if the neural changes


wrought by mid-cycle hormonal status reduce stress
Study (by first

responses in a way that has behavioral influence,


one would expect these women to have displayed
author)

Wang

less anxiety or other negative emotions than when in


Zuo

the early follicular phase. Yet this was not the case,
Is there Neurosexism in Functional Neuroimaging? 397

either before or after viewing seventy-two highly although for a third meta-analytic study that eliminates
arousing aversive pictures. all studies without male comparisons and/or that use
These two speculations, both based on extremely preexisting mathematics scores as a covariate, and
small sample sizes, are of particular note given the comes to a different conclusion, see 101]. This is just
long history of prejudice against women based on the one example of the general phenomenon that social
supposed psychological effects of their hormones [8]. context affects gendered behavior in myriad ways [for
Considered together, they also illuminate the problem- numerous other examples, see 10]. Clearly, such social
atic nature of a piecemeal approach to research. How, influences have neural correlates.
for example, would the amygdala of the fertile hetero- The implication of this for researchers is that the
sexual female be expected to respond to an attractive effects of gendered experiences or situations on brain
but potentially dangerous male? Would it be predicted development or function are (literally) incorporated
to show a greater response to facilitate more effective into a sex difference in neural activity. Thus a single
flirtation, or reduced response to facilitate boldness in ‘snap-shot’ comparison of male/female brain activity
the social interaction? is uninformative as to the extent to which any neuro-
logical sex differences (and any concomitant behav-
ioral differences) are due to the effects of experience
Exaggeration of Fixedness? Plasticity of Brain on brain development and function, versus the mani-
and Mind festation of fixed, stable and universal male/female
neural signatures [18]. Importantly, while a ‘snap-
A third important issue when it comes to interpreting shot’ approach to research doesn’t explicitly endorse
sex differences in the brain is the potential plasticity of the idea of fixed sex differences in the brain (and
sex differences in both brain and mind. Neural circuit- behavior), such an approach can neither produce data
ry develops through, and is altered by, experience to challenge such an interpretation, nor illuminate or
[e.g., 87–90], and this has been shown to be the case support any other account of how behavioral sex dif-
even for low-level sex differences in the rat brain [91, ferences might arise. Conversely, a ‘plasticity’ ap-
for discussion of this point and its neglect in research, proach that devotes attention to the neural correlates
see 92]. As a number of feminist scientists have point- of the known malleability of sex differences in behav-
ed out, gendered life experiences and social construc- ior could potentially do so. Thus, if charges of neuro-
tions of gender (such as leisure activities, educational sexism are incorrect, researchers should avoid over-
interests, poverty and status) have material effects on reliance on simple ‘snap-shot’ comparisons.
the body, including the brain [e.g., 12, 93–95]. Mean- To investigate whether this was the case, each study
while, behavioral sex differences have often been from the previously used sample was categorised as
shown to vary by historical period, culture, demo- taking a ‘plasticity’ approach if it examined whether
graphic factors, ethnicity, and even in response to potentially relevant gender-related experiences (such as
subtle social cues. To take the example of mathemat- masculine or feminine occupations, educational history
ics, in the United States the gender gap in mean or past-times), social factors (such as socio-economic
mathematical performance at school has reduced and background or marital status) or context (such as pres-
closed over the past few decades, while the sex differ- ence or absence of stereotype threat in the portrayal of
ence at very high levels of mathematical performance the task) moderated sex differences in brain activity.
has been found to vary across time and place as well as Otherwise, it was categorised as ‘snap-shot’. All 39
across ethnicities within North America [96–98]. In studies took a ‘snap-shot’ approach to research.
addition, social psychological research indicates that
mathematical performance can vary within the same
individual across different social contexts. For exam- Discussion
ple, investigations of the ‘stereotype threat’ phenome-
non find that female mathematical performance is The brain science of male/female difference has an
improved when, for instance, tests are presented in a unfortunate history of neurosexism, in which scientif-
way that de-emphasizes or makes irrelevant the ste- ically unjustified claims furnished support for tradi-
reotype that females are poor at maths [99, 100, tional gender stereotypes and roles. Some have
398 C. Fine

recently argued that FNI investigations of sex differ- scientific warrant. In short, the picture revealed from
ences largely follow that tradition. Conversely, others these three investigations was one in which evidentia-
have responded to such criticisms with claims that ry standards are tolerant of both the production and
they over-emphasize the peril of such research, at the persistence of false-positive claims of sex differences.
expense of the current and future promise. This article The second approach to judging the validity of the
examined the navigation of three obstacles to obtain- two perspectives of the literature looked at how
ing valuable information about sex differences, as a researchers typically navigate the functional obscurity
way of illuminating the validity of these two differing of brain differences, and the room for gender
perspectives. stereotype-infused speculations this allows. The extent
First, treatment of the scope for false-positive errors to which researchers speculated on, rather than sys-
in FNI sex differences research was systematically tematically investigated, the psychological signifi-
explored in three ways: typical sample sizes, a case cance of sex differences in brain activity was
study, and citation practices. Analysis of a recent two investigated in the same recent sample of FNI studies.
year (2009 and 2010) sample found that findings of None of the thirty-nine studies tested a prediction
sex differences in fMRI investigations are predomi- based on an explicit neurocognitive model of sex-
nantly reported in studies with inadequate sample modulated mental processes subserving the behavior
sizes. Nearly three quarters of studies had 15 or fewer of interest. Over two-thirds of the studies speculated
participants of each sex in each of their subgroups of on psychological differences in the sexes on the basis
interest, and for approximately a fifth of the studies of neurological findings, all but three doing so either
there were fewer than ten. Empirically based analyses in the absence of supporting behavioral data or in the
of group differences arising from samples of this size presence of contradictory data. While caution and
indicate low reliability, sensitivity, and generalizability restraint were in evidence in a number of studies, it
[38, 42], a point underlined by the example of reports was still the case that post hoc reverse inferences were
of sex differences in language lateralization discussed more common than not. This is not surprising since,
previously [37, 43, 44]. That the majority of reported ultimately, such research is intended to illuminate psy-
sex differences involve studies with low statistical chological differences between the sexes. Yet when
power that compare groups with fewer than 16 partic- such speculative reverse inferences are not part of
ipants suggests that there is not great concern, in systematic model building, the scope for influence of
general, as to the possibility that claims of sex differ- erroneous gender stereotypes is high. This was espe-
ences in brain activations may be spurious. Second, cially clear in cases in which speculations were con-
treatment of the scope for false positive errors was also sistent with gender stereotypes but inconsistent with
investigated with an examination of standards of evi- the researchers’ own behavioral data.
dence for a recent claim of sex differences in the brain Finally, using the same sample, researchers’ atten-
described as responsibly made [21], beyond reason- tion to the potential plasticity of sex differences in
able doubt [49] and of sufficient warrant to be cited brain and mind was investigated. Studies were cate-
without caveat in some expert reviews [e.g., 52]. This gorised on the basis of whether they explored the
found that only two supporting studies directly com- potential plasticity of sex differences in brain activity
pared the sexes, and one of these suffered from sample by looking at how factors such as systematically gen-
selection bias. Both had small sample sizes and dered experiences, demographic factors or social con-
reflected ambiguity as to how to construct the depen- text might contribute to, or moderate, sex difference in
dent variable. Finally, concern with respect to false- brain activation; or whether they relied on a single
positive errors was investigated in a third way by ‘snap-shot’ of male/female difference. All 39 studies
looking at recent citations of a sex difference in lan- took a ‘snap-shot’ approach.
guage lateralization for which considerable contradic- These findings seem to render untenable claims that
tory data exists, including two meta-analyses. Fifty- charges of neurosexism in scientific research are mis-
seven per cent of citing authors did not refer to the placed; at least with regards to the FNI literature. The
presence of any contradictory data, and fewer than a long-noted publication bias toward positive findings
third cited one or both meta-analyses, approximately of sex differences is exacerbated by tolerance for
half doing so in a way that did not indicate its greater positive findings from sample sizes that yield low
Is there Neurosexism in Functional Neuroimaging? 399

reliability and generalizability, as well as less than that could contradict the notion that gender is entirely
ideal citation practices. While a report of a sex differ- socially constructed.
ence in the brain, even if erroneous, does not neces- There are social, as well as scientific, reasons for
sarily support gender stereotypes (particularly given the neuroscientific community to acknowledge the
the possibility that neural differences may have no validity of feminist criticisms of the research: argu-
behavioral significance), functional interpretations of ably, the relatively subtle forms of neurosexism iden-
apparent neurological sex differences are common, tified here contribute to the more egregious versions
and little effort appears to be devoted to the develop- that appear in the popular literature. Recently, a num-
ment of neurocognitive models to constrain and test ber of scientists have drawn attention to the harmful
such speculations to avoid gender stereotype-infused effects of popular neurosexism in reinforcing gender
interpretations. Lastly, a predominantly static ‘snap- stereotypes [e.g., 9, 10, 21, 104, 105]. Yet research is
shot’ approach to research guarantees that no data that currently being conducted in a way that biases the
challenge the implicit assumption of fixed male/fe- literature towards presenting neurological sex differ-
male neural signatures will be found, and that the ences as numerous, functionally significant, and fixed.
processes underlying experiential contributions to, Thus, even adequately accurate popular dissemination
and plasticity of, neurological or behavioral gender of the neuroscientific research literature would be
differences remain unexplored. Together, these com- biased towards interpretations that implicitly reify the
mon neuroscientific research practices bias the scien- status quo.
tific literature toward a presentation of sex differences Moreover, neuroscientists could also usefully con-
in the brain as “essential”; that is extensive, function- sider other ways in which research may contribute to,
ally significant in gender stereotypically consistent and license, popular forms of neurosexism. First, the
ways, and fixed. greater the volume of false-positive errors that exist in
It might be objected that the conclusion to be drawn the literature, the more scope there is for popular
from the information presented here is that cognitive writers to make claims about sex differences in the
neuroimaging, like all science, is imperfect—not that brain that will ultimately prove to be false. Clearly,
it is sexist. It is certainly true that issues such as false- false-positive results are inevitable, but the scope for
positive errors, within-group analyses, citation bias, them is greatly increased by current common practi-
and logically and empirically unpersuasive reverse ces. In addition, the scientific community itself does
inferences are hardly unique to sex differences re- not always set a good example in terms of how such
search [39, 45, 102, 103]. However, that these prob- findings should be treated. Eliot [104], for example,
lems affect FNI investigations and behavioral science has recently rightly criticized popular writers for
more generally is not grounds to dismiss charges of cherry-picking spurious findings, using as an example
neurosexism. The reason this objection fails is a fea- references in the popular media to Shaywitz et al.’s
ture of the research so obvious that it is all-but invis- finding of greater male lateralization, despite the null
ible: theoretically, the science could carry exactly the conclusion of the two meta-analytic investigations of
same flaws but be biased in precisely the opposite the hypothesis. Yet as noted earlier, the same phenom-
way. Thus, in theory, it could be false-positive claims enon is present in more than half of recent citations in
of the effects of gender socialization (rather than the scientific literature itself. A similar argument
biological sex) on brain activity that are facilitated applies to functional interpretations of supposed
through common research practices. Similarly male/female brain differences. While some claims
researchers could, on the basis of ambiguous neuro- made by popular writers appear to be the products of
logical findings, frequently speculate about the psy- enviably potent imaginations, in other instances
chological effects of socialization or context on they are recognisable (albeit exaggerated and over-
gendered behavior in a piecemeal fashion that is not confident) versions of hypotheses, interpretations and
developed into explicit neurocognitive models and speculations made by researchers themselves [see 10].
systematically tested. Lastly, researchers could rou- Anecdotally, scientists have a reputation for over-
tinely neglect to investigate the influence of biological cautiousness in the statements they are prepared to
sex on neural activity during the performance of gen- make, thus it seems plausible that the propensity of
dered tasks, guaranteeing that no data are produced scientists to make such speculations, to draw on
400 C. Fine

gender stereotypes to do so, and to fail to test them First, scientific progress is not served by the prolif-
systematically (and thus potentially reject them), will eration of false-positive errors, the premature accep-
increase the ease and apparent appropriateness for tance of hypotheses, or the perpetuation of false-
popular commentators to make such speculations positive findings through citing practices. Second, al-
themselves. Finally, a number of scientists have ap- though exploratory research and post hoc speculation
propriately criticized popular writers for false asser- clearly have important roles in science, to reduce
tions that any sex differences observed in the brain scope for unsubstantiated reverse inferences and, more
must be ‘innate’ or fixed [e.g., 10, 21, 104]. Yet the generally, better serve scientific progress, this should
‘snap-shot’ research approach implicitly reinforces— lead to the systematic development and testing of
or at the very least fails to challenge—the notion of neurocognitive models of sex differences. In an inter-
fixed male/female neural signatures. If the neuroscien- esting observation that spans both these issues, Bluhm
tific literature were full of studies exploring the [14] has pointed out that a statistical technique known
plasticity of sex differences in the brain—how, for as region-of-interest (ROI) analysis, in which brain
example, they vary across time, culture, socioeconomic activity differences are sought in pre-specified regions
status, gendered experience, social context, and so on— of the brain, is common in this area of research.
popular writers would be less able to assume or assert Because ROI analyses involve far fewer comparisons
that supposed neurological differences are ‘hardwired’. than whole brain analyses, researchers are able to
In line with this point, Eliot [105] has recently argued lower statistical thresholds for significance. While
that neuroscientists should pay more attention to gender the aim is to increase the chance of finding a group
enculturation processes in the brain. The current find- difference, it also increases the risk of false-positive
ings strongly reinforce this suggestion. error. Moreover, because ROI analyses examine only
It is of course not suggested that scientists bear isolated regions of the brain, Bluhm notes that they
blanket responsibility for popular representations of serve to act against the development of sophisticated
their work, and their responsibility at the popular neurocognitive models, which require an understand-
interface is a difficult question beyond the scope of ing of the functional relationships of the entire brain
this article. However, in the face of evidence of the network involved in such tasks, and the relation of
manifestation of neurosexism in the scientific research different parts of the network to differences in behav-
itself, it behoves the scientific community to consider ior. Thus, the decision to use this analysis technique
their contribution to popular scientific understanding implicitly prioritizes the finding of a sex difference
of gender through the proliferation of false-positive over theoretical advance and the avoidance of false-
errors [see also 106], untested stereotype-consistent positive errors.
reverse inferences, and lack of attention to the poten- Third, similar arguments can be made as to the
tial plasticity of sex differences. benefit of taking into account criticism of the lack of
Then, there are scientific reasons for the neurosci- attention to the plasticity of sex differences. In humans
entific community to acknowledge the validity of especially, gendered behavior shows substantial
feminist critiques. Concerns that the influence of such within-group variation that is influenced by factors
criticisms on neuroscientists may “hinder” or even such as historical period, nationality, experience and
“reverse” [22] scientific progress seem entirely mis- social context. Neuroscientific research will only con-
placed. FNI investigations of sex differences can im- tribute to rich explanations of gender if research is
prove in their service of the internal goal of science, guided by a sophisticated conceptual understanding
which is to establish reliable and valuable knowledge of the phenomenon. As Springer, Stellman and
about nature. It is worth noting that none of the fem- Jordan-Young have recently argued, “measures of
inist critics cited here have suggested, as a solution to sex are not pristine, but include effects of gender”
this, the termination of such research: to argue that the [93, p. 1] meaning that insights into gender differences
research is often flawed is not equivalent to arguing require going “[b]eyond a catalogue of differences” to
that it should not be done at all. To the contrary, taking instead investigate the biological mechanisms that in-
heed of charges of neurosexism in each of the three teract with gendered experiences, by which differen-
domains discussed would serve to improve the quality ces between sexes arise. Jordan-Young & Rumiati [13]
of the science. have recently made recommendations along such lines
Is there Neurosexism in Functional Neuroimaging? 401

for brain research, suggesting greater exploration of Clements-Stephens, A.M., S.L. Rimrodt, and L.E.
neural plasticity, as well as into the ways variation Cutting. 2009. Developmental sex differences
arising from other social categories—such as social in basic visuospatial processing: Differences in
class, occupation, and nationality—impact gender strategy use? Neuroscience Letters 449(3):
differences. As they point out, such a research 155–160.
approach “might provide much more illumination Coman, I.L., M.H. Gnirke, F.A. Middleton, K.M.,
on the concrete mechanisms through which the Antshel, W. Fremont, A.M. Higgins, et al.
social world shapes behavior, and even becomes 2010. The effects of gender and catechol O-
embodied (brain) difference” (p. 23). methyltransferase (COMT) Val108/158Met
In short, it is hard to see how taking heed of charges polymorphism on emotion regulation in
of neurosexism could possibly impede scientific prog- velo-cardio-facial syndrome (22q11.2 dele-
ress in this area. To the contrary, it should hasten it. In tion syndrome): An fMRI study. Neuro-
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