Are Sex-Related Category-Specific Differences in Semantic Tasks Innate or Influenced by Social Roles?

A Viewpoint

Guido Gainotti, MD

Abstract: In semantic tasks, sex-related categorical differences, in the form of better processing of fruits and vegetables by
women and of artifacts (human-made objects) and animals by men, have been reported both in healthy participants and in
brain-damaged patients. Researchers’ interpretation of these sex-related categorical asymmetries has, however, been con-
troversial, being connected with the more general (innatist ver-sus experience-dependent) interpretations that had been
given of the mechanisms subsuming the categorical organization of the brain. I begin this review with a brief reminder of
the debate between supporters of the innatist and the experience-related accounts of categorical brain organization. Then I
summarize results that have documented a preference by women for fruits and vegetables and a preference by men for
artifacts and ani-mals, and I discuss the innatist and social role-related inter-pretations that have been given of these results.
I conclude that sex-related categorical effects disappear in generations in which the traditional social roles have almost
completely disappeared, and these differences are not seen in young individuals raised in societies that emphasize sex
equality.

Key Words: sex-related categorical effects, animal versus plant-life categories, innatist model, traditional social roles,
genera-tional and cultural factors

(Cogn Behav Neurol 2017;30:43–47)

Data concerning sex differences in cognitive abilities in healthy participants were first summarized by Maccoby and
Jacklin in their classic 1974 book The Psychology of Sex Differences. In 1977, McGlone wrote a seminal paper showing
that aphasia is far more frequent in men than in women. Since then, studies have prolif-erated on sex-related cognitive
differences, both in healthy participants and in brain-damaged patients. There are now hundreds of studies about sex
differences in cognitive abilities, showing that men outperform women in overall spatial abilities, while women outperform
men in overall

Received for publication October 24, 2016; accepted March 6, 2017. From the Institute of Neurology, Universita`Cattolica
del Sacro Cuore,

and IRCCS [Istituto di Ricovero e Cura a Carattere Scientifico] Fondazione Santa Lucia, Department of Clinical and
Behavioral Neurology, Rome, Italy.
The author declares no conflicts of interest.

Reprints: Guido Gainotti, MD, Institute of Neurology, Catholic University of Rome, Largo A. Gemelli, 8, 00168 Rome,
Italy (e-mail: gainotti@rm.unicatt.it).
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Cogn Behav Neurol Volume 30, Number 2, June 2017

verbal ability (see Halpern, 2012, for a comprehensive review).

All these differences have generally been explained in evolutionary terms. Thus, Geary (1998) maintained that developing
superior navigation skills may have en-abled men to become better suited to the role of hunters, and that women’s superior
verbal skills may have enabled women to use language to gain social advantage, as by argument and persuasion.

Some authors have questioned these evolutionary explanations. For instance, Weiss et al (2003) stressed the relevance of
sociocultural factors, educational factors, and training to the observed sex differences. More recently, other, subtler kinds
of sex-related cognitive differences have been consistently reported in the neuropsychological literature. These differences
concern category-specific effects (see Gainotti et al, 2010, for a review).
According to these studies, healthy women gen-erally show a greater familiarity and proficiency than men in recognizing
members of plant-life categories (flowers, fruits, vegetables), whereas healthy men generally exhibit a preference for tools
and other artifacts (ie, human-made objects) and for animals (Gainotti et al, 2010; Laiacona et al, 2006). A similar
asymmetry is shown in patients with brain damage, who are more impaired with items in the less familiar categories:
Women show a prevalent defect in recognizing artifacts and animals, and men show a greater impairment than women in
recognizing flowers, fruits, and vegetables (Gainotti, 2005, 2010).

The interpretation that researchers have given to these sex-related categorical asymmetries has often been consistent with
Geary’s (1998) evolutionary account of the sex-related differences in cognitive abilities and, in any case, has shared the
more general (innatist versus experience-dependent) interpretations that had been given of the mech-anisms subsuming the
categorical organization of the brain.

Before we can undertake a meaningful and sys-tematic survey of sex-related category-specific effects and their underlying
mechanisms, we need to remember how the debate between supporters of the innatist and of the experience-related
accounts of categorical brain organ-ization originated and have evolved over time.

CATEGORY-SPECIFIC SEMANTIC DISORDERS AND THE “DIFFERENTIAL WEIGHTING” HYPOTHESIS

Warrington and colleagues (Warrington and McCarthy, 1983, 1987; Warrington and Shallice, 1984) first advanced the

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Gainotti Cogn Behav Neurol Volume 30, Number 2, June 2017

hypothesis that conceptual knowledge, instead of being evenly distributed across the cerebral cortex, may be organized by
categories and that its disruption may be category-specific. Warrington and Shallice (1984) found that in four patients who
had herpes simplex encephalitis lesions involving the anterior parts of the temporal lobes, semantic impairment
preferentially disrupted the biological categories of animals, fruits, and vegetables. By contrast, Warrington and McCarthy
(1983, 1987) observed that in two patients with vascular lesions involving the left frontotemporoparietal cortices, tools and
other artifact categories were more affected than were items belonging to biological categories.

These authors also noted that the patients’ semantic disorders did not respect the boundaries between bio-logical and
artifact categories. For instance, the body parts category tended to be disrupted in association with artifacts, whereas the
musical instruments category tended to be disrupted in association with biological items. The authors explained their
findings through the facts that our knowledge of animals and musical instru-ments is based on a similar prevalence of
visual and acoustic information, while our knowledge of body parts and tools (and other artifacts) is based more on actions
and somatosensory information. These conclusions were supported by Gainotti’s (2000, 2015) reviews of later studies.

The more general inference that could be drawn from these observations was that “category-specific se-mantic disorders”
must be considered the by-product of a basic dichotomy concerning the “differential weighting” that visuoperceptual and
functional attributes have in the representation of biological and artifact categories, rather than as the result of disruption of
true biological and artifact categories.

According to the “differential weighting” model, biological categories would be jointly disrupted because members of
these categories are differentiated mainly through subtle visuoperceptual features such as the plain, striped, or spotted skin
that distinguishes a lion from a tiger or a leopard. Tools and other artifacts are dis-tinguished more by the different
functions for which hu-man beings created them, and knowledge about them is based more on actions and somatosensory
information than on their visual features.

This interpretation has been substantially confirmed by investigations of healthy people using feature lists (eg, Cree and
McRae, 2003; Ventura et al, 2005; Vigliocco et al, 2004; Vinson et al, 2003) or using Likert scales to evaluate the influence
of different perceptual and motor activities in the mental representation of biological and artifact categories (eg, Gainotti et
al, 2009, 2013; Hoffman and Lambon Ralph, 2013; Tranel et al, 1997). Indeed, these studies have consistently shown that:
The visual modality is usually considered the main source of knowledge for all (biological and artifact) categories.

In biological categories, the most important source of knowledge after vision is other perceptual modalities, but in artifact
categories it is the actions performed with the objects.

The “differential weighting” hypothesis, besides being in keeping with these data gathered in healthy participants, could
also explain the neuroanatomic cor-relates of category-specific semantic disorders affecting the biological and artifact
categories: a bilateral impair-ment of the anterior temporal lobes in category-specific semantic disorders for biological
entities, and a lesion of the left frontotemporoparietal cortices in disorders mainly concerning tools and other artifacts.

The anterior parts of the temporal lobes were se-lectively damaged in the patients with herpes simplex encephalitis
described by Warrington and Shallice (1984) and in many more recently reported patients with category-specific semantic
disorders for biological entities (for surveys, see Capitani et al, 2003, and Gainotti, 2000, 2005). The anterior temporal
lobes are, indeed, a locus of convergence of the ventral stream of visual processing with auditory, olfactory, and gustatory
inputs. This ex-plains why biological entities are mainly represented in these parts of the brain (Gainotti et al, 2013).

The dorsal stream of visual processing converges with body-related and action-oriented structures in the frontoparietal
sensorimotor cortices. This could explain why left frontoparietal areas play a major role in the representation of artifacts
(Buxbaum and Saffran, 2002; Buxbaum et al, 2007).

A different degree of lateralization of the brain representations of biological entities and artifacts can be explained by the
fact that the major sources of knowledge of biological entities (ie, visual and other perceptual in-puts) are bilaterally
represented, but the action-oriented structures that provide an important source of knowledge about artifacts are mainly
represented in the left hemi-sphere, which controls the movements of the right side of the body.

CARAMAZZA AND THE HYPOTHESIS OF AN INNATE CATEGORICAL ORGANIZATION OF CONCEPTUAL

KNOWLEDGE

Caramazza and colleagues (eg, Capitani et al, 2003; Caramazza, 1998; Caramazza and Mahon, 2006; Caramazza and
Shelton, 1998; Mahon and Caramazza, 2003) addressed several objections to the “differential weighting” hypothesis and
assumed an innate categorical organization of conceptual knowledge, which they called the “domains of knowledge
hypothesis.” According to this innatist model, category-specific impairments for animals (potential predators), plant life
(possible sources of food), and artifacts reflect the disruption of innate brain networks shaped by natural selection to
support rapid identification of objects that are crucial for survival.

Some support for this position has come from dis-sociations within the biological categories, because some reported
category-specific semantic disorders mainly affect animals (eg, Blundo et al, 2006; Caramazza and Shelton, 1998; De
Renzi and Lucchelli, 1994; Hart and Gordon, 1992) or plant life (eg, Capitani et al, 2009; Goldenberg, 1992; Hart et al,
1985; Humphreys and Riddoch, 2003; Kensinger et al, 2003; Samson and Pillon, 2003).

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Cogn Behav Neurol Volume 30, Number 2, June 2017 Social Roles and Sex-Related Category-Specific Differences

In two review papers aiming to clarify whether the anatomic locus of a lesion is different in disorders specific to animal
versus plant-life categories or whether other factors can account for these dissociations within the bi-ological categories,
Gainotti (2005, 2010) concluded that two factors, related, respectively, to sex and to the lesion of rostral or caudal parts of
the ventral stream of visual processing, could account for the differences between patients with category-specific disorders
for animals and plant life. A prevalent impairment of plant-life categories was most likely in men who had a lesion in the
territory of the left posterior cerebral artery, encroaching upon the occipital and the inferomesial aspects of the left
temporal lobe. A prevalent impairment of animals was most likely in women with a bilateral lesion of the anterior temporal
cortices.

Gainotti showed that the size of the sex effect was significant. In his first (2005) review, 24 of 35 brain-injured men (68%)
were mainly impaired at naming fruits and vegetables, while 12 of 13 brain-injured women (92%) were mostly impaired at
naming animals. The sex effect was even more pronounced in Gainotti’s sec-ond (2010) review: 20 of 21 brain-injured
men (95%) showed a greater impairment for fruits and vegetables than for animals, while nine of 11 brain-injured women
(80%) showed a greater impairment for animals.

This effect was not unexpected. Several authors had already documented an interaction between sex and fa-miliarity with
different kinds of biological and artifact categories. For instance, significant sex-related asymme-tries for biological and
artifact categories had been ob-served in normal participants by investigators gathering normative naming data from adults
and children (Funnell et al, 2006; McKenna and Parry, 1994), evaluating familiarity ratings for various categories
(Albanese et al, 2000), and studying the age of acquisition of common names (Barbarotto et al, 2008; Funnell et al, 2006).

McKenna and Parry (1994) had found sex-related asymmetries in normative naming data from adults and children; male
participants scored higher with animals and small manipulable objects, but female participants scored higher with fruits
and vegetables. Funnell et al (2006) had obtained similar data studying the age at which people acquire common names.
Albanese et al (2000) had found that healthy women gave higher familiarity ratings to fruits, vegetables, and furniture, and
healthy men to tools. Barbarotto et al (2008) had shown that healthy boys had earlier acquisition than healthy girls of the
names of stimuli in the categories of tools and vehicles.

Similar asymmetries had been found by Laws (1999, 2000, 2004) on speeded naming and identification tasks and on name
generation tasks. Laws (1999) examined the naming latencies of normal undergraduate students to pictures of biological
and artifact items, and confirmed a sex-by-category interaction, with the women being slower than the men to name artifact
items and the men slower to name biological entities. Laws also showed that women made more errors on artifacts than
men in a naming-to-deadline paradigm (Laws, 2000) and on name generation

tasks (Laws, 2004). In this last study he examined four semantic categories (animals, tools, fruits, and vehicles) and found
an advantage of women with fruits and of men with tools.

Similar sex-related asymmetries about biological and artifact categories on other semantic fluency tasks have been reported
by Capitani et al (1999) and Cameron et al (2008). Like Laws (2004), Capitani et al (1999) found that women retrieved
more names of fruits, whereas men fared better with tools. Cameron et al (2008) found that women named significantly
more fruit and furniture items, while men named more tools.

Finally, on an object decision task, Barbarotto et al (2002) found a sex-by-category interaction, with a female superiority
with fruits and vegetables and a male ad-vantage with artifacts.

In all these studies, men were more familiar with artifacts and women with biological entities, particularly fruits and
vegetables. Furthermore, and more in keeping with the results of Gainotti’s (2005, 2010) reviews, a de-tailed analysis of
data gathered in normal participants suggested a further sex-by-category interaction within biological categories, because
men were more proficient with animals and women with fruits and vegetables.

These sex-related dissociations within the biological categories, with strong recognition of animals only by men, were
observed not just in McKenna and Parry’s (1994) normative naming data study, but also by Marra et al (2007), Cameron et
al (2008), and Moreno-Martı´nez and Moratilla-Pe´rez (2016). Marra et al (2007) showed that men were more fluent with
the birds category and women with the furniture category. On a semantic fluency task, Cameron et al (2008) showed that
younger women named more fruits and older men named more animals than did their sex-matched peers. Moreno-Martı
´nez and Moratilla-Pe´rez (2016), comparing animals, vegetables, and artifacts on a naming task, showed that young men
were more accurate than young women at naming ani-mals and artifacts.

ATTEMPTS TO RECONCILE SEX-RELATED EFFECTS TO INNATIST MODELS VERSUS EXPERIENCE-

RELATED MODELS OF CATEGORICAL BRAIN ORGANIZATION
Laws (2000, 2004) tried to reconcile these sex effects with inborn models of categorical brain organization, and his attempt
was further developed by Laiacona et al (2006).

Laws (2000, 2004) proposed that the main historical subsistence activities of men (hunting) and women (gathering) may
have spurred the greater development of brain circuits dealing with tools and animals in men and with fruits and vegetables
in women.

Laiacona et al (2006) developed this line of thought and suggested that the evolutionary pressures that, according to
Caramazza and coworkers (eg, Caramazza, 1998; Caramazza and Mahon, 2006; Mahon and Caramazza, 2003), had
prompted the development of different brain

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Gainotti Cogn Behav Neurol Volume 30, Number 2, June 2017

networks dedicated to animals, plant life, and tools, might have also provided each sex with more efficient cognitive
representations of their main working and foraging targets (ie, tools and animals for men and fruits and vegetables for
women).

This inborn account of sex effects based on evolu-tionary pressures is, however, at variance with the fact that sex effects do
not respect the boundaries among the artifacts, animals, and plant-life categories contemplated by the “domains of
knowledge hypothesis.” Some authors (eg, Albanese et al, 2000; Gainotti et al, 2013; Moreno-Martı´nez et al, 2008) have
shown, for instance, that in the artifact categories, men fare better with tools and women with furniture and kitchen
utensils.

A different, experience-dependent interpretation of sex-related asymmetries was, therefore, proposed by Gainotti (2005,
2010) and by Marra et al (2007). These authors explained the sex effects based on the greater familiarity that men might
have with tools and with certain kinds of animals (probably because they are more involved in hunting), and on women’s
greater familiarity with fruits and vegetables (probably because of their cooking).

This suggestion was partially confirmed by Scotti et al (2010), who collected familiarity ratings from normal men and
women for 288 animals, subdividing them ac-cording to whether they were hunted or fished, and showed that men were
more familiar with hunted animals.

The hypothesis that sex-related asymmetries may be experience-dependent seemed, however, at variance with results
obtained in young men and women by Moreno-Martı´nez et al (2008), studying semantic fluency in different subcategories
of biological and artifact items, and by Gainotti et al (2010) assessing young men and women’s familiarity with different
biological and artifact categories. Neither study found differences between the young men and young women on any of the
tested categories.

THE POSSIBLE INFLUENCE OF GENERATIONAL AND CULTURAL FACTORS ON SEX-RELATED CATEGORY-

SPECIFIC EFFECTS

The unexpected results of Moreno-Martı´nez et al (2008) and Gainotti et al (2010) may be explained by the participants
having been undergraduate students, who belong to a generation in which the traditional social roles have almost
completely disappeared.

An argument in favor of this point came from an-other part of the Moreno-Martı´nez et al (2008) study, in which a group of
elderly participants showed differences consistent with the importance of social role-related fa-miliarity factors. The
elderly women showed greater flu-ency for flowers, vegetables, and kitchen utensils, and the elderly men showed better
fluency for musical instruments. The other artifact subcategories showed nonsignificant differences in the directions
suggested by the social-role hypothesis, such as a greater fluency of the elderly men for tools and of the elderly women for
furniture.
Gainotti et al (2013) had similar findings when they assessed the familiarity of young and elderly men and

46 | www.cogbehavneurol.com

women with various semantic categories by presenting plant, animal, and artifact categories in words or in pic-tures. The
results confirmed the hypothesis of a genera-tional difference in fluency: The elderly (but not the young) women showed a
greater familiarity with flowers than the elderly men, and the elderly (but not the young) men were much more familiar
with animals than the elderly women.

Gerlach and Gainotti (2016) used an alternative method of testing the hypothesis that sex-related cat-egory-specific effects
have an evolutionary origin. The authors argued that the hypothesis could be disproved by showing that sex differences do
not exist in cultures that do not stress different social roles for men and women. They chose to conduct a study in
Denmark, a country that encourages sex equality. They recruited a large sample of young adults and gave them two tasks,
the “difficult object decision” and “superordinate classi-fication” tasks. According to Gerlach (2009), these two tasks can
produce reliable category effects in neuro-logically intact participants. Despite the sensitive nature of the tasks, Gerlach
and Gainotti (2016) found no evi-dence of sex differences in the processing of the examined categories, and argued that
previous reports of sex dif-ferences had probably reflected differences in familiarity originating from socially based sex
roles.

CONCLUDING REMARKS

This survey clearly shows that sex-related category-specific effects are not innate, but arise from personal experiences
linked to social roles.

It must be noted, however, that these results cannot be generalized to two broader questions:

These results cannot address the issue of whether categorical brain organization is inborn or experience-dependent,
because even inborn models acknowledge the importance of experience in shaping brain organization.

These results cannot affect the controversy over whether sex asymmetries are innate or related to social roles, because I
have shown only that sex-related cognitive asymmetries for specific categorical domains are strongly influenced by sex-
related social roles.

Different conclusions could be reached by taking into account more general cognitive (eg, verbal versus visuospatial),
emotional, affective, and prosocial (eg, Espinosa and Kova´rˇı´k, 2015) sex-related differences.

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