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 An Evolutionary Perspective of Sex-Typed Toy Preferences: Pink, Blue, and the Brain
 Journal article by Gerianne M. Alexander; Archives of Sexual Behavior, Vol. 32, 2003
An evolutionary perspective of sex-typed toy preferences: pink, blue,
and the brain.
by Gerianne M. Alexander
Large sex differences in toy preferences exist throughout much of childhood (for
discussion, see Ruble & Martin, 1998) and appear to further sex differences in cognitive
and social development. Playthings, selected to amuse or engage the interest of a child,
also afford opportunities for object manipulation or exploration that appear to enhance
sex-dimorphic spatial abilities (Liss, 1981). Most children prefer playmates of the same
sex and with compatible play styles (e.g., Alexander & Hines, 1994), and these
preferences result in same-sex groupings that promote sex-dimorphic social interaction
patterns (Maccoby, 1990, 1998). In these ways, sex-dimorphic toy preferences in
childhood are early underpinnings of gender role in adulthood.
This paper describes research on sex differences in human behavior and perceptual
processing suggesting that evolved visual processing biases contribute to contemporary
sex-dimorphic toy preferences. This new suggestion is consistent with the general
hypothesis that contemporary sex-dimorphic play styles may have adaptive significance
for males and females. For example, selection pressures for male bonds that facilitated
successful group hunting and protection of resources are thought to have evolved male
preferences for male playmates (Benenson, Morganstein, & Roy, 1998). Research
reviewed in this paper suggests that the early social roles of males and females may also
have evolved preferences for object features and functions that influence children's toy
preferences and perpetuate behavioral sex differences with adaptive significance. As
summarized below, the proposed transactional relations among biological factors, social
roles of males and females, and toy preferences are supported by studies on the prox
imate social and biological determinants of toy preferences and research on the
evolutions of sex-dimorphic spatial abilities and color vision.
PROXIMATE SOCIAL AND BIOLOGICAL INFLUENCES ON CHILDREN'S TOY
PREFERENCES
Children's toy preferences are often explained in terms of gender socialization. A gender
label clearly initiates a process of social learning that includes modeling and
reinforcement of sex-typical toy preferences (Bussey & Bandura, 1999). Consistent
with the stereotypical social roles of men and women, male infants are provided more
frequently with toy vehicles or toy tools, whereas female infants are provided more
frequently with dolls (Pomerleau, Bolduc, Malcuit, & Cossette, 1990). In later
development, boys and girls prefer different toys (Connor & Serbin, 1977; Liss, 1981)
and these toy preferences are consistent with the general cultural view of gender
appropriate toys. The apparent internalization of social norms for gender appropriate
toys is thought to occur with the formation of a gender identity--the hypothesized core
of gender schemas or mental representations that include socially defined gender
appropriate behavior (Maccoby, 1988; Martin, 1989, 1999; Martin & Halverson, 1981;
Martin & Little, 1 990). From this perspective, once a child accepts membership in a
gender group, he or she comes to value and adopt the social role associated with their
gender label, and this gender role includes preferences for toys such as dolls or vehicles.
A gender label is initiated by the dichotomous categorization of the external genitalia,
whose male or female appearance is one outcome of a cascade of prenatal hormonal
processes that also influences the sex-dimorphic development of the brain, at least in
nonhuman mammals (Kelly, Ostrowski, & Wilson, 1999; MacLusky, Bowlby, Brown,
Peterson, & Hochberg, 1997). Increasingly, studies on human and nonhuman animal
species indicate that another outcome of this biological process of sexual differentiation
is sex-dimorphic behaviors. Experimental manipulation of gonadal hormones (e.g., by
physical or chemical castration or by injecting exogenous androgens) during nonhuman
development shows unequivocally that hormone dependent masculinization of the brain
increases the frequency of subsequent rough and tumble play (Meaney, 1988; Meaney
& McEwen, 1986) and also masculinizes sexual and aggressive behavior (Breedlove,
Cooke, & Jordan, 1999; Cooke, Hegstrom, Villeneuve, &Breedlove, 1998). Studies on
atypical reproductive development during prenatal life in humans suggest that sex
differences in prenatal androgen levels may initiate similar behavioral sex-dimorphisms
in our postnatal life (Collaer & Hines, 1995; Wilson, 1999)--tendencies that in typical
development appear amplified by gender socialization (e.g., Campbell & Eaton, 1999).
Girls with congenital adrenal hyperplasia, for example, are exposed to high levels of
adrenal androgens prenatally (i.e., more male-typical; e.g., Carson et al., 1982). Some
research indicates that postnatally they show greater aggression (Berenbaum & Resnick,
1997), enhanced (i.e., masculine) visuospatial abilities (Hampson, Rovet, & Altmann,
1998; Resnick, Berenbaum, Gottesman, & Bouchard, 1986), more masculine
occupational preferences (Berenbaum, 1999), and an increased rate of bisexual or
homosexual sexual orientation in fantasy and/or behavior (Zucker et al., 1996).
Preferences for toys typically preferred by boys are also increased in androgenized girls
(Berenbaum & Hines, 1992; Hines & Kaufman, 1994). Increased preferences for
"masculine" toys may indicate an atypical gender socialization of androgenized girls
(Fausto-Sterling, 1992). They also suggest that biological factors (i.e., prenatal levels of
androgens) may influence sex-dimorphic toy preferences (Berenbaum & Hines, 1992;
Hines & Kaufman, 1994). In view of animal research indicating prenatal androgens
promote rough and active play (e.g., Meaney, 1988), one previous suggestion is that
higher levels of prenatal androgens in girls may increase preferences for "masculine"
toys because such objects afford greater opportunities for engaging in male-typical play
(e.g., Hines & Kaufman, 1994). Biological influences on toy preferences are also
consistent with other research showing that visual preferences in infants for gender-
linked toys exist earlier in development than predicted by cognitive--social theories of
gend er role behavior (Campbell, Shirley, & Heywood, 2000; O'Brien & Huston, 1985;
Serbin, Poulin-Dubois, Colburne, Sen, & Eichstedt, 2001). Moreover, as visual
preferences for gender-linked toys precede an ability to engage in gender-linked play-
styles, sex differences in the salience or rewarding properties of distinct object features
associated with "masculine" or "feminine" toys appear to exist (Campbell et al., 2000).
An innate preference for distinct object features would also explain why vervet
monkeys (Cerecopithecus aethiops sabaeus) show sex differences in toy preferences
similar to those documented previously in children (Alexander & Hines, 2002). In that
study, the proportion of contact time with toys typically preferred by boys (a car and a
ball) was greater in male vervets compared to female vervets, whereas the proportion of
contact time with toys typically preferred by girls (a doll and a pot) was greater in
female vervets compared to male vervets. Sex-dimorphic object preferences in infants
and in nonhuman primates suggest that the conceptual category of "masculine" or
"feminine" is directed by aperceptual category of female-preferred and male-preferred
objects. If so, then "masculinized" toy preferences in androgenized girls (e.g., Hines &
Kaufman, 1994) may occur, in part' because prenatal androgen levels influence the
structure and function of the brain systems that subserve the recognition of these object
c ategories.
VISUAL PROCESSING BIASES APPEAR TO INFLUENCE SEX-DIMORPHIC
TOY PREFERENCES
Different perceptual features appear to categorize male-preferred and female-preferred
objects. Male-preferred toys such as vehicles have been described as objects with an
ability to be used actively (O'Brien & Huston, 1985), to be observed moving in space,
or to promote a movement characterized by propulsion (Benenson, Liroff, Pascal, &
Cioppa, 1997). In free drawings, boys are more likely to depict these objects in global
spatial arrangements (e.g., bird's eye view; Minamoto, 1985). Female-preferred toys
have been described previously as objects, like dolls, that afford opportunities for
nurturance (Campbell et al., 2000; Eisenberg, Murray, & Hite, 1982; Miller, 1987). In
free drawings, girls tend to depict people or smaller natural details (i.e., flowers) in row
arrangements. Compared to boys, girls are also more likely to use a greater number of
colors and to prefer warmer colors (i.e., pink and red) to cooler colors (i.e., blue and
green; Minamoto, 1985). In toy choices and free drawings, then, boys appear to assign
greater attention or interest to object movement and location, whereas girls appear to
assign greater attention or interest to form and color.
There is a correspondence between the perceptual features that appear to characterize
male-preferred and female-preferred objects (and children's representations of such
objects) and the well-established processing efficiencies of the two visual pathways. In
humans and nonhuman primates, anatomical, physiological, and behavioral evidence
indicates two anatomically and functionally distinct pathways or processing streams
originate in the magnocellular (M) and parvocellular (P) retinal ganglion cells and
project to the frontal cortex (Kastner & Ungerleider, 2000; Ungerleider & Mishkin,
1982). Compared to the P-cell pathway, the M-cell pathway is phylogenetically older
(Livingstone & Hubel, 1987) and both anatomical (e.g., Burkhalter, Bernardo, &
Charles, 1993) and behavioral evidence (e.g., Kovacs, 2000) suggests that the M-cell
processing stream develops in advance of the P-cell processing stream. Object
recognition, the identification of visual patterns and red--green but not blue--yellow
colors (e.g., Hendry & Reid, 2000) are processed through the P-cell pathway (the
"what" pathway) that proceeds ventrally from the parvocellular subdivision of the
lateral geniculate nucleus to the inferior temporal region of the brain. Spatial location,
object movement, and a global analysis of visual scenes are processed through the M-
cell pathway (the "where" pathway) that proceeds dorsally from the magnocellular
subdivision of the lateral geniculate nucleus to the posterior parietal cortex (Kastner &
Ungerleider, 2000; Livingstone & Hubel, 1988; Ungerleider & Mishkin, 1982). The
anatomical and functional separation of the two subcortical pathways is well established
(e.g., Livingstone & Hubel, 1988; Merigan & Maunsell, 1993). The development and
degree of the functional separation of the two pathways at the cortical level, however, is
a subject of current investigation and debate (e.g., Born, 2001; Dobkins & Anderson,
2002; Merigan & Maunsell, 1993).
The apparent correspondence between the characteristics of "masculine" and "feminine"
toys and the information provided by the two visual processing pathways implicates
visual processing pathways in the recognition and development of gender-linked toy
preferences. If so, then findings that girls exposed prenatally to high levels of androgens
show masculinized toy preferences (e.g., Hines & Kaufman, 1994) suggest that
androgens may promote the sex-dimorphic development of the visual processing
pathways, a possibility supported by recent research of the retina. The retina (the origin
of the magnocellular and parvocellular ganglion cells) in the rat is a sex-dimorphic
structure, such that retinal thickness in males compared to females increases in the
perinatal period (Salyer, Lund, Fleming, Lephart, & Horvath, 2001). Androgens
aromatized to estrogens in the rat retina masculinize that structure (Salyer et al., 2001),
similar to the sex-dimorphic development of other brain structures (MacLusky et al.,
1997). Est rogen receptors exist in the human retina (Ogueta, Schwartz, Yamashita, &
Farber, 1999), consistent with the recent proposal that the postnatal surge of testicular
androgens in males of a variety of mammalian species (Corbier, Edwards, & Roffi,
1992) may masculinize the retina and associated visual pathways, thereby promoting
sex-dimorphic visuospatial abilities (Salyer et al., 2001).
Other findings in studies on primates are consistent with androgen-dependent effects on
visual processing pathway structure at the level of the cortex. In infant rhesus moneys, a
female advantage in object discrimination is abolished by castration of males because
testicular androgens appear to suppress the maturation of the temporal cortex (i.e., part
of the ventral pathway) in nonhuman primates (Bachevalier & Hagger, 1991). Similarly,
the earlier onset of stereopsis and binocularity in girls compared to boys (Bauer,
Shimojo, Gwizada, & Held, 1986), coupled with findings of positive correlations
between testosterone levels and the onset of these abilities in male infants (Held, Bauer,
& Gwiazda, 1988), have suggested that the postnatal surge of testicular androgens may
influence neuronal connectivity of the human visual cortex. Finally, sex differences in
the functional efficiencies of these two pathways in later development are indicated by
findings that boys compared to girls show a greater global perceptu al bias (Kramer,
Ellenberg, Leonard, & Share, 1996), consistent with a male bias (or specialization) for
M-cell pathway processing. In contrast, girls compared to boys show an advantage for
object discrimination (similar to that observed in rhesus monkeys; Overman,
Bachevalier, Schuhmann, & Ryan, 1996) and for color naming (Bornstein, 1985),
consistent with a female bias (or an earlier specialization) for P-cell pathway
processing.
The ventral visual processing stream, and in particular the temporal cortex, is also
implicated in processing facial features (Nelson, 2001). Therefore, findings that girls
and women compared to boys and men show an advantage in processing facial
expressions (for review, see McClure, 2000) also support the existence of sex-
dimorphic visual processing biases. In early development, infants generally show
preferences for faces over patterned stimuli (e.g., Fantz, 1963). They also generally
prefer moving objects over stationary objects (Nelson & Horowitz, 1987). However,
when presented with an object with mechanical movement and a human face with
natural movement, 1-day-old boys show a larger visual preference for the object with
mechanical movement (i.e., a mobile), whereas girls of that age show a larger visual
preference for the female face (Connellan, Baron-Cohen, Wheelwright, Batki, &
Ahluwalia, 2000). These results suggest that sex-dimorphic visual preferences
consistent with M-cell or P-cell processing ef ficiencies precede experience with
gender-linked objects (e.g., trucks or dolls). Neonatal visual preferences (along with the
apparent recognition of sex-typed toy categories by infants and the masculinized toy
preferences of girls with atypical androgen exposure during prenatal development)
support the hypothesis that androgens may initiate the specialization of visual pathways
that contribute to visual biases for object movement or form/color.
Compared to adults, the segregation of the anatomical and functional properties of the
M-cell and P-cell pathways at the cortical level is less pronounced in infants (Dobkins
& Anderson, 2002), consistent with the proposal that parcellation (i.e., selective loss of
synapses and dendrites in the cortex) and specialization of visual processing streams is
directed by experience in postnatal life (Johnson, 2001). The tendency for newborns to
orient to faces, for example, is argued to reflect an innate bias mediated by the
subcortical visual pathways (Johnson & Morton, 1991; Morton & Johnson, 1991). This
visual bias at birth ensures that developing cortical circuits are preferentially exposed to
faces, which provides the necessary learning experiences that shape the further
development of cortical brain areas specialized for face-identification (Johnson, 2001).
This bidirectional interaction between the structure and function of visual processes is
consistent with the current proposal that sex differences in an i nnate tendency to attend
to movement or color/form direct a child's interest to gender-linked objects, such as
toys, and suggest further that these gender-linked experiences may organize brain
circuits that promote sex-dimorphic processing efficiencies. From this perspective, sex-
dimorphic toy preferences may arise from androgen-dependent effects on the visual
system, but gender socialization may provide the required experiences that further the
development of brain areas that contribute to sex differences in cognitive (i.e.,
visuospatial abilities) and social (i.e., face processing) behavior.
DISTAL FACTORS APPEAR TO HAVE INFLUENCED SEC-DIMORPHIC
VISUAL PATHWAY PROCESSING EFFICIENCIES IN HUMANS
Research on the adaptive significance of sex-dimorphic spatial abilities and color vision
suggests that the early social roles of women and men evolved sex differences in M-cell
(motion) and P-cell (object form and color) pathway function. Evolutionary theorists
(Eals & Silverman, 1994; Silverman & Eals, 1992) have reasoned that selection
pressures might have contributed to spatial abilities in men that enhanced the hunt and
capture of animals, such as the identification of spatial position and movement.
Similarly, they have proposed selection pressures might have contributed to abilities in
females that enhanced the foraging of plant food, such as the identification of form and
color and memory for object-landmark associations (Eals & Silverman, 1994;
Silverman & Eals, 1992). The adaptive significance of processing spatial position and
movement (i.e., information provided by the M-cell pathway; e.g., Ungerleider &
Mishkin, 1982) for males is consistent with the contemporary male advantage in spatial
navigat ion (Galea & Kimura, 1993; Moffat, Harnpson, & Hatzipantelis, 1998;
Silverman et al., 2000) and the accurate aim of projectiles (Watson & Kimura, 1991). In
addition, tasks developed to measure the processing requirements of gathering (Eals &
Silverman, 1994), which are consistent with information provided by the P-cell pathway
(Alexander, Packard, & Peterson, 2002), show that women and young girls outperform
men and young boys in their memory for objects identities and their relative locations in
a visual spatial array (Alexander et al., 2002; Eals & Silverman, 1994; Silverman &
Eals, 1992).
Research on the evolution of color vision also supports an association between the early
social role of women and an evolved female advantage or specialization for processing
the visual information provided by the P-cell pathway, in this instance red-green colors.
Open areas and objects differ substantially in the degree to which they reflect ultraviolet
light, consistent with speculation that early color vision was favored by selection
because discrimination between open spaces and objects facilitated an identification of
food sources (Pichaud, Briscoe, & Desplan, 1999). In humans and related primates, this
primordial color subsystem is the yellow-blue system (Nathans, 1999). Research on
foraging in contemporary nonhuman primates (e.g., Dominy & Lucas, 2001) supports
the hypothesis that the human evolution of the second red-green system may have
furthered food gathering ability because it facilitated, for example, the identification of
ripe, yellow fruit from a surround of green foliage (e.g., Nathans, 1999 ; Regan et al.,
2001) and edible red leaves among unripe green foliage (Dominy & Lucas, 2001).
Consistent with this interpretation of the adaptive significance of color vision for
foraging, memory scores in humans for object locations in a visual array (i.e., a
gathering analogue task that typically shows a female advantage) appear enhanced when
objects are red on a green background compared to green on red background (Hellige &
Cumberland, 2001; Roth & Hellige, 1998).
Whereas discrimination of red wavelengths appears to facilitate identification of plant
food, a preference for red or pink appears to have an advantage for successful female
reproduction. In research on nonhuman primates (Higley, Hopkins, Hirsch, Marra, &
Suomi, 1987), a female preference for "reddish-pink" compared to yellow or green is
thought to exist because infant faces compared to adult faces are reddish-pink, and red
or pink may signal approach behaviors that enhance infant survival. In addition, women
and men appear able to use the spectral properties of the human face for gender
discrimination (males being more red; females being more green; Tarr, Kersten, Cheng,
& Rossion, 2001), suggesting that a female preference for red may also have promoted
recognition and approach to males. Thus, the social role of early females (i.e., foraging
for plant food and caretaking of infants) may have evolved in girls compared to boys a
greater specialization for color processing and a greater preference for objects with a
pink or reddish color.
In humans, apes, and Old World monkeys normal color vision depends on three types of
photoreceptors (i.e., cones) that contain retinal photopigments that absorb light
maximally at low, medium, or high wavelengths. In humans, these wavelengths
correspond to the labels blue (S or short wave), green (M or mid wave), and red (L or
long wave; Mollon, 1986). Human color vision is trichromatic because all other colors
we perceive are determined by stimulation of one or more of these three cones and by
the strength of stimulation that is received. The primordial yellow-blue system is
transmitted on an autosomal gene, whereas red-green sensitivity is transmitted on the X
chromosome (Mollon, 1986; Nathans, Thomas, & Hogness, 1986). Males, having one X
chromosome--and so only one set of red-green system genes--are more likely than
females to be color deficient (Mollon, 1986). In contrast, women are more likely than
men to have evolved a fourth retinal photopigment that permits even greater
differentiation of colors (Ja meson, Highnote, & Wasserman, 2001), consistent with the
observed female advantage in sex-dimorphic color behavior (e.g., Bornstein, 1985). In
humans (Morgan, Adam, & Mollon, 1992) and in nonhuman primates (Shyue et al.,
1995), dichromats (who are more frequently males) are better able to detect texture and
color-camouflaged objects. These empirical findings have suggested color-blindness
may be adaptive for detecting and evading predation (Shyue et al., 1995). The genetic
basis of color vision, therefore, is consistent with the speculation that color vision and,
in particular the ability to discriminate red wavelengths, may have a greater adaptive
significance for foragers (i.e., females) than for resource protectors (i.e., males) and so
contribute to contemporary visual biases and object preferences. The recent finding that
sex-dimorphic object preferences appear to exist in a nonhuman primate species
(Alexander & Hines, 2002), suggests that, like color vision, sex-dimorphic object
preferences appear to hav e arisen early in human evolution, prior to the emergence of a
distinct hominid lineage.
CONCLUSIONS
There is increasing evidence that the brain has evolved specialized recognition systems
for categories that have adaptive significance, such as emotional expressions and facial
identity (for discussion, see Duchaine, Cosmides, & Tooby, 2001). In view of the
evidence summarized above, it seems possible that males and females have also evolved
specialized visual biases that optimize the development of sex-dimorphic behaviors
with adaptive significance. The adaptive significance of spatial abilities consistent with
hunting for males suggests that the male visual system (and in particular the M-cell
pathway) is highly sensitive or responsive to objects that provide experience with
tracking spatial movements of objects. This novel hypothesis is consistent with the
proposal that toys, such as balls or cars, are more interesting to males than to females
because they elicit motion (e.g., Eisenberg et al., 1982). If the female visual system (and
in particular the P-cell pathway) has evolved to better forage for food or promote
caretaking of infants, then female infants may be biologically prepared to be highly
sensitive or responsive to object features--in particular color. Girls' preferences for dolls
and warm colors (e.g., Iijima, Arisaka, Minamoto, & Arai, 2001) and a female
advantage in facial expression processing (McClure, 2000) are all consistent with this
possibility.
This theory of sex-typed toy preferences predicts that parametric manipulation of those
variables associated with the processing efficiencies of the different visual pathways
(e.g., texture, spatial frequency, movement) will produce sex-specific effects on the
visual preferences of infants and the toy preferences of older children. Further, given
that infants appear to use perceptual features, such as vocal pitch (Miller, Younger, &
Morse, 1982) to categorize males and females, it may be useful to consider whether the
early development of color vision in infancy (Bornstein, Kessen, & Weiskopf, 1976;
Teller, 1998) also provides information that contributes to gender category knowledge--
and whether this information is more salient to girls than to boys. Moreover, if
aromatized androgens influence visual processing pathway development in humans,
then androgenized girls compared to typically developing girls may show more
masculinized patterns of visual development (e.g., later color naming, poorer object
discrim ination, visual preferences for mechanical movement). Recent findings that
androgenized girls show in free drawings more of the perceptual features associated
with boys' drawings (i.e., attention to object movement and location) and fewer of the
perceptual features associated with girls' drawings (i.e., attention to form and color;
Iijima et al., 2001) are consistent with this possibility. Similarly, atypical toy
preferences are an early feature of the atypical development of sex-dimorphic behavior
(e.g., gender identity dysphoria, adult homosexual orientation; Bailey & Zucker, 1995;
Zucker & Bradley, 1995), suggesting the gender-typical early organization of the visual
processing pathways may be altered--perhaps by hormone effects during early postnatal
development or by experiences with gender-linked objects during early infancy. If so,
then male children with gender identity disorder, for example, may show feminized
patterns of visual development (e.g., earlier color naming, greater color discrimination,
b etter face processing). Whereas the sexual differentiation of the periphery (i.e.,
genitals) may be a primary determinant of gender socialization, early preferences for
object characteristics may be an empirical window to a sex-typed "temperament," a
product of the sexual differentiation of the central nervous system that evolved to
predispose an interest in stimuli that promote the acquisition of a gender identity and
gender role.
Evolutionary psychology holds that an individual processes and experiences the
external world as constrained by the survival and reproduction of the species (Bjorklund
& Pellegrini, 2000). Accordingly, a transactional relation between a maturing individual
and a changing environment is the formative force behind our developing cognitive
strategies and abilities. Evolutionary theory is a challenge to understand the complex
interplay between nature and culture, in the context of a more distal determinant of
behavior, namely, natural selection. From this perspective, it seems that an association
between toy preferences and gender role behavior may be mediated by sex differences
in visual processing that evolved from the social roles of early males and females and
are organized by hormones in perinatal development. Although hormones may organize
structures that predispose an interest in object features, the general bidirectional theory
of brain structure and brain function (Johnson & Morton, 1991) predicts that g ender
socialization provides the required experiences that direct the sex-dimorphic
specialization of the two visual processing streams. Thus, in view of the evolution of the
phylogenetically older yellow--blue opponent system (Nathan, 1999) and the X-linked
green--red opponent system (Mollon, 1986; Nathans et al., 1986), it may be more than a
trivial coincidence that in our current culture we assign blue to boys and pink to girls.
ACKNOWLEDGMENTS
I thank Mark G. Packard and Bradley S. Peterson for helpful comments on an earlier
version of the paper.
Received December 4, 2001; revisions received April 8, 2002, and May 21, 2002;
accepted May 21, 2002
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Gerianne M. Alexander, Ph.D. (1,2)
(1.) Yale Child Study Center, New Haven, Connecticut.
(2.) To whom correspondence should be addressed at Department or Psychology, Texas
A&M University, 5235-TAMU, College Station, Texas 77843-4235; e-mail:
gma@psyc.tamu.edu.
-1-
Questia Media America, Inc. www.questia.com
Publication Information:Article Title: An Evolutionary Perspective of Sex-Typed Toy Preferences: Pink, Blue, and the
Brain. Contributors: Gerianne M. Alexander - author. JournalTitle: Archives of SexualBehavior. Volume: 32. Issue: 1.
Publication Year: 2003. Page Number: 7+. COPYRIGHT 2003 Plenum Publishing Corporation; COPYRIGHT 2003 Gale
Group

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An evolutionary perspective of sex typed toy preferences

  • 1.  An Evolutionary Perspective of Sex-Typed Toy Preferences: Pink, Blue, and the Brain  Journal article by Gerianne M. Alexander; Archives of Sexual Behavior, Vol. 32, 2003 An evolutionary perspective of sex-typed toy preferences: pink, blue, and the brain. by Gerianne M. Alexander Large sex differences in toy preferences exist throughout much of childhood (for discussion, see Ruble & Martin, 1998) and appear to further sex differences in cognitive and social development. Playthings, selected to amuse or engage the interest of a child, also afford opportunities for object manipulation or exploration that appear to enhance sex-dimorphic spatial abilities (Liss, 1981). Most children prefer playmates of the same sex and with compatible play styles (e.g., Alexander & Hines, 1994), and these preferences result in same-sex groupings that promote sex-dimorphic social interaction patterns (Maccoby, 1990, 1998). In these ways, sex-dimorphic toy preferences in childhood are early underpinnings of gender role in adulthood. This paper describes research on sex differences in human behavior and perceptual processing suggesting that evolved visual processing biases contribute to contemporary sex-dimorphic toy preferences. This new suggestion is consistent with the general hypothesis that contemporary sex-dimorphic play styles may have adaptive significance for males and females. For example, selection pressures for male bonds that facilitated successful group hunting and protection of resources are thought to have evolved male preferences for male playmates (Benenson, Morganstein, & Roy, 1998). Research reviewed in this paper suggests that the early social roles of males and females may also have evolved preferences for object features and functions that influence children's toy preferences and perpetuate behavioral sex differences with adaptive significance. As summarized below, the proposed transactional relations among biological factors, social roles of males and females, and toy preferences are supported by studies on the prox imate social and biological determinants of toy preferences and research on the evolutions of sex-dimorphic spatial abilities and color vision. PROXIMATE SOCIAL AND BIOLOGICAL INFLUENCES ON CHILDREN'S TOY PREFERENCES Children's toy preferences are often explained in terms of gender socialization. A gender label clearly initiates a process of social learning that includes modeling and
  • 2. reinforcement of sex-typical toy preferences (Bussey & Bandura, 1999). Consistent with the stereotypical social roles of men and women, male infants are provided more frequently with toy vehicles or toy tools, whereas female infants are provided more frequently with dolls (Pomerleau, Bolduc, Malcuit, & Cossette, 1990). In later development, boys and girls prefer different toys (Connor & Serbin, 1977; Liss, 1981) and these toy preferences are consistent with the general cultural view of gender appropriate toys. The apparent internalization of social norms for gender appropriate toys is thought to occur with the formation of a gender identity--the hypothesized core of gender schemas or mental representations that include socially defined gender appropriate behavior (Maccoby, 1988; Martin, 1989, 1999; Martin & Halverson, 1981; Martin & Little, 1 990). From this perspective, once a child accepts membership in a gender group, he or she comes to value and adopt the social role associated with their gender label, and this gender role includes preferences for toys such as dolls or vehicles. A gender label is initiated by the dichotomous categorization of the external genitalia, whose male or female appearance is one outcome of a cascade of prenatal hormonal processes that also influences the sex-dimorphic development of the brain, at least in nonhuman mammals (Kelly, Ostrowski, & Wilson, 1999; MacLusky, Bowlby, Brown, Peterson, & Hochberg, 1997). Increasingly, studies on human and nonhuman animal species indicate that another outcome of this biological process of sexual differentiation is sex-dimorphic behaviors. Experimental manipulation of gonadal hormones (e.g., by physical or chemical castration or by injecting exogenous androgens) during nonhuman development shows unequivocally that hormone dependent masculinization of the brain increases the frequency of subsequent rough and tumble play (Meaney, 1988; Meaney & McEwen, 1986) and also masculinizes sexual and aggressive behavior (Breedlove, Cooke, & Jordan, 1999; Cooke, Hegstrom, Villeneuve, &Breedlove, 1998). Studies on atypical reproductive development during prenatal life in humans suggest that sex differences in prenatal androgen levels may initiate similar behavioral sex-dimorphisms in our postnatal life (Collaer & Hines, 1995; Wilson, 1999)--tendencies that in typical development appear amplified by gender socialization (e.g., Campbell & Eaton, 1999). Girls with congenital adrenal hyperplasia, for example, are exposed to high levels of adrenal androgens prenatally (i.e., more male-typical; e.g., Carson et al., 1982). Some research indicates that postnatally they show greater aggression (Berenbaum & Resnick, 1997), enhanced (i.e., masculine) visuospatial abilities (Hampson, Rovet, & Altmann, 1998; Resnick, Berenbaum, Gottesman, & Bouchard, 1986), more masculine
  • 3. occupational preferences (Berenbaum, 1999), and an increased rate of bisexual or homosexual sexual orientation in fantasy and/or behavior (Zucker et al., 1996). Preferences for toys typically preferred by boys are also increased in androgenized girls (Berenbaum & Hines, 1992; Hines & Kaufman, 1994). Increased preferences for "masculine" toys may indicate an atypical gender socialization of androgenized girls (Fausto-Sterling, 1992). They also suggest that biological factors (i.e., prenatal levels of androgens) may influence sex-dimorphic toy preferences (Berenbaum & Hines, 1992; Hines & Kaufman, 1994). In view of animal research indicating prenatal androgens promote rough and active play (e.g., Meaney, 1988), one previous suggestion is that higher levels of prenatal androgens in girls may increase preferences for "masculine" toys because such objects afford greater opportunities for engaging in male-typical play (e.g., Hines & Kaufman, 1994). Biological influences on toy preferences are also consistent with other research showing that visual preferences in infants for gender- linked toys exist earlier in development than predicted by cognitive--social theories of gend er role behavior (Campbell, Shirley, & Heywood, 2000; O'Brien & Huston, 1985; Serbin, Poulin-Dubois, Colburne, Sen, & Eichstedt, 2001). Moreover, as visual preferences for gender-linked toys precede an ability to engage in gender-linked play- styles, sex differences in the salience or rewarding properties of distinct object features associated with "masculine" or "feminine" toys appear to exist (Campbell et al., 2000). An innate preference for distinct object features would also explain why vervet monkeys (Cerecopithecus aethiops sabaeus) show sex differences in toy preferences similar to those documented previously in children (Alexander & Hines, 2002). In that study, the proportion of contact time with toys typically preferred by boys (a car and a ball) was greater in male vervets compared to female vervets, whereas the proportion of contact time with toys typically preferred by girls (a doll and a pot) was greater in female vervets compared to male vervets. Sex-dimorphic object preferences in infants and in nonhuman primates suggest that the conceptual category of "masculine" or "feminine" is directed by aperceptual category of female-preferred and male-preferred objects. If so, then "masculinized" toy preferences in androgenized girls (e.g., Hines & Kaufman, 1994) may occur, in part' because prenatal androgen levels influence the structure and function of the brain systems that subserve the recognition of these object c ategories. VISUAL PROCESSING BIASES APPEAR TO INFLUENCE SEX-DIMORPHIC TOY PREFERENCES
  • 4. Different perceptual features appear to categorize male-preferred and female-preferred objects. Male-preferred toys such as vehicles have been described as objects with an ability to be used actively (O'Brien & Huston, 1985), to be observed moving in space, or to promote a movement characterized by propulsion (Benenson, Liroff, Pascal, & Cioppa, 1997). In free drawings, boys are more likely to depict these objects in global spatial arrangements (e.g., bird's eye view; Minamoto, 1985). Female-preferred toys have been described previously as objects, like dolls, that afford opportunities for nurturance (Campbell et al., 2000; Eisenberg, Murray, & Hite, 1982; Miller, 1987). In free drawings, girls tend to depict people or smaller natural details (i.e., flowers) in row arrangements. Compared to boys, girls are also more likely to use a greater number of colors and to prefer warmer colors (i.e., pink and red) to cooler colors (i.e., blue and green; Minamoto, 1985). In toy choices and free drawings, then, boys appear to assign greater attention or interest to object movement and location, whereas girls appear to assign greater attention or interest to form and color. There is a correspondence between the perceptual features that appear to characterize male-preferred and female-preferred objects (and children's representations of such objects) and the well-established processing efficiencies of the two visual pathways. In humans and nonhuman primates, anatomical, physiological, and behavioral evidence indicates two anatomically and functionally distinct pathways or processing streams originate in the magnocellular (M) and parvocellular (P) retinal ganglion cells and project to the frontal cortex (Kastner & Ungerleider, 2000; Ungerleider & Mishkin, 1982). Compared to the P-cell pathway, the M-cell pathway is phylogenetically older (Livingstone & Hubel, 1987) and both anatomical (e.g., Burkhalter, Bernardo, & Charles, 1993) and behavioral evidence (e.g., Kovacs, 2000) suggests that the M-cell processing stream develops in advance of the P-cell processing stream. Object recognition, the identification of visual patterns and red--green but not blue--yellow colors (e.g., Hendry & Reid, 2000) are processed through the P-cell pathway (the "what" pathway) that proceeds ventrally from the parvocellular subdivision of the lateral geniculate nucleus to the inferior temporal region of the brain. Spatial location, object movement, and a global analysis of visual scenes are processed through the M- cell pathway (the "where" pathway) that proceeds dorsally from the magnocellular subdivision of the lateral geniculate nucleus to the posterior parietal cortex (Kastner & Ungerleider, 2000; Livingstone & Hubel, 1988; Ungerleider & Mishkin, 1982). The anatomical and functional separation of the two subcortical pathways is well established
  • 5. (e.g., Livingstone & Hubel, 1988; Merigan & Maunsell, 1993). The development and degree of the functional separation of the two pathways at the cortical level, however, is a subject of current investigation and debate (e.g., Born, 2001; Dobkins & Anderson, 2002; Merigan & Maunsell, 1993). The apparent correspondence between the characteristics of "masculine" and "feminine" toys and the information provided by the two visual processing pathways implicates visual processing pathways in the recognition and development of gender-linked toy preferences. If so, then findings that girls exposed prenatally to high levels of androgens show masculinized toy preferences (e.g., Hines & Kaufman, 1994) suggest that androgens may promote the sex-dimorphic development of the visual processing pathways, a possibility supported by recent research of the retina. The retina (the origin of the magnocellular and parvocellular ganglion cells) in the rat is a sex-dimorphic structure, such that retinal thickness in males compared to females increases in the perinatal period (Salyer, Lund, Fleming, Lephart, & Horvath, 2001). Androgens aromatized to estrogens in the rat retina masculinize that structure (Salyer et al., 2001), similar to the sex-dimorphic development of other brain structures (MacLusky et al., 1997). Est rogen receptors exist in the human retina (Ogueta, Schwartz, Yamashita, & Farber, 1999), consistent with the recent proposal that the postnatal surge of testicular androgens in males of a variety of mammalian species (Corbier, Edwards, & Roffi, 1992) may masculinize the retina and associated visual pathways, thereby promoting sex-dimorphic visuospatial abilities (Salyer et al., 2001). Other findings in studies on primates are consistent with androgen-dependent effects on visual processing pathway structure at the level of the cortex. In infant rhesus moneys, a female advantage in object discrimination is abolished by castration of males because testicular androgens appear to suppress the maturation of the temporal cortex (i.e., part of the ventral pathway) in nonhuman primates (Bachevalier & Hagger, 1991). Similarly, the earlier onset of stereopsis and binocularity in girls compared to boys (Bauer, Shimojo, Gwizada, & Held, 1986), coupled with findings of positive correlations between testosterone levels and the onset of these abilities in male infants (Held, Bauer, & Gwiazda, 1988), have suggested that the postnatal surge of testicular androgens may influence neuronal connectivity of the human visual cortex. Finally, sex differences in the functional efficiencies of these two pathways in later development are indicated by findings that boys compared to girls show a greater global perceptu al bias (Kramer, Ellenberg, Leonard, & Share, 1996), consistent with a male bias (or specialization) for
  • 6. M-cell pathway processing. In contrast, girls compared to boys show an advantage for object discrimination (similar to that observed in rhesus monkeys; Overman, Bachevalier, Schuhmann, & Ryan, 1996) and for color naming (Bornstein, 1985), consistent with a female bias (or an earlier specialization) for P-cell pathway processing. The ventral visual processing stream, and in particular the temporal cortex, is also implicated in processing facial features (Nelson, 2001). Therefore, findings that girls and women compared to boys and men show an advantage in processing facial expressions (for review, see McClure, 2000) also support the existence of sex- dimorphic visual processing biases. In early development, infants generally show preferences for faces over patterned stimuli (e.g., Fantz, 1963). They also generally prefer moving objects over stationary objects (Nelson & Horowitz, 1987). However, when presented with an object with mechanical movement and a human face with natural movement, 1-day-old boys show a larger visual preference for the object with mechanical movement (i.e., a mobile), whereas girls of that age show a larger visual preference for the female face (Connellan, Baron-Cohen, Wheelwright, Batki, & Ahluwalia, 2000). These results suggest that sex-dimorphic visual preferences consistent with M-cell or P-cell processing ef ficiencies precede experience with gender-linked objects (e.g., trucks or dolls). Neonatal visual preferences (along with the apparent recognition of sex-typed toy categories by infants and the masculinized toy preferences of girls with atypical androgen exposure during prenatal development) support the hypothesis that androgens may initiate the specialization of visual pathways that contribute to visual biases for object movement or form/color. Compared to adults, the segregation of the anatomical and functional properties of the M-cell and P-cell pathways at the cortical level is less pronounced in infants (Dobkins & Anderson, 2002), consistent with the proposal that parcellation (i.e., selective loss of synapses and dendrites in the cortex) and specialization of visual processing streams is directed by experience in postnatal life (Johnson, 2001). The tendency for newborns to orient to faces, for example, is argued to reflect an innate bias mediated by the subcortical visual pathways (Johnson & Morton, 1991; Morton & Johnson, 1991). This visual bias at birth ensures that developing cortical circuits are preferentially exposed to faces, which provides the necessary learning experiences that shape the further development of cortical brain areas specialized for face-identification (Johnson, 2001). This bidirectional interaction between the structure and function of visual processes is
  • 7. consistent with the current proposal that sex differences in an i nnate tendency to attend to movement or color/form direct a child's interest to gender-linked objects, such as toys, and suggest further that these gender-linked experiences may organize brain circuits that promote sex-dimorphic processing efficiencies. From this perspective, sex- dimorphic toy preferences may arise from androgen-dependent effects on the visual system, but gender socialization may provide the required experiences that further the development of brain areas that contribute to sex differences in cognitive (i.e., visuospatial abilities) and social (i.e., face processing) behavior. DISTAL FACTORS APPEAR TO HAVE INFLUENCED SEC-DIMORPHIC VISUAL PATHWAY PROCESSING EFFICIENCIES IN HUMANS Research on the adaptive significance of sex-dimorphic spatial abilities and color vision suggests that the early social roles of women and men evolved sex differences in M-cell (motion) and P-cell (object form and color) pathway function. Evolutionary theorists (Eals & Silverman, 1994; Silverman & Eals, 1992) have reasoned that selection pressures might have contributed to spatial abilities in men that enhanced the hunt and capture of animals, such as the identification of spatial position and movement. Similarly, they have proposed selection pressures might have contributed to abilities in females that enhanced the foraging of plant food, such as the identification of form and color and memory for object-landmark associations (Eals & Silverman, 1994; Silverman & Eals, 1992). The adaptive significance of processing spatial position and movement (i.e., information provided by the M-cell pathway; e.g., Ungerleider & Mishkin, 1982) for males is consistent with the contemporary male advantage in spatial navigat ion (Galea & Kimura, 1993; Moffat, Harnpson, & Hatzipantelis, 1998; Silverman et al., 2000) and the accurate aim of projectiles (Watson & Kimura, 1991). In addition, tasks developed to measure the processing requirements of gathering (Eals & Silverman, 1994), which are consistent with information provided by the P-cell pathway (Alexander, Packard, & Peterson, 2002), show that women and young girls outperform men and young boys in their memory for objects identities and their relative locations in a visual spatial array (Alexander et al., 2002; Eals & Silverman, 1994; Silverman & Eals, 1992). Research on the evolution of color vision also supports an association between the early social role of women and an evolved female advantage or specialization for processing the visual information provided by the P-cell pathway, in this instance red-green colors. Open areas and objects differ substantially in the degree to which they reflect ultraviolet
  • 8. light, consistent with speculation that early color vision was favored by selection because discrimination between open spaces and objects facilitated an identification of food sources (Pichaud, Briscoe, & Desplan, 1999). In humans and related primates, this primordial color subsystem is the yellow-blue system (Nathans, 1999). Research on foraging in contemporary nonhuman primates (e.g., Dominy & Lucas, 2001) supports the hypothesis that the human evolution of the second red-green system may have furthered food gathering ability because it facilitated, for example, the identification of ripe, yellow fruit from a surround of green foliage (e.g., Nathans, 1999 ; Regan et al., 2001) and edible red leaves among unripe green foliage (Dominy & Lucas, 2001). Consistent with this interpretation of the adaptive significance of color vision for foraging, memory scores in humans for object locations in a visual array (i.e., a gathering analogue task that typically shows a female advantage) appear enhanced when objects are red on a green background compared to green on red background (Hellige & Cumberland, 2001; Roth & Hellige, 1998). Whereas discrimination of red wavelengths appears to facilitate identification of plant food, a preference for red or pink appears to have an advantage for successful female reproduction. In research on nonhuman primates (Higley, Hopkins, Hirsch, Marra, & Suomi, 1987), a female preference for "reddish-pink" compared to yellow or green is thought to exist because infant faces compared to adult faces are reddish-pink, and red or pink may signal approach behaviors that enhance infant survival. In addition, women and men appear able to use the spectral properties of the human face for gender discrimination (males being more red; females being more green; Tarr, Kersten, Cheng, & Rossion, 2001), suggesting that a female preference for red may also have promoted recognition and approach to males. Thus, the social role of early females (i.e., foraging for plant food and caretaking of infants) may have evolved in girls compared to boys a greater specialization for color processing and a greater preference for objects with a pink or reddish color. In humans, apes, and Old World monkeys normal color vision depends on three types of photoreceptors (i.e., cones) that contain retinal photopigments that absorb light maximally at low, medium, or high wavelengths. In humans, these wavelengths correspond to the labels blue (S or short wave), green (M or mid wave), and red (L or long wave; Mollon, 1986). Human color vision is trichromatic because all other colors we perceive are determined by stimulation of one or more of these three cones and by the strength of stimulation that is received. The primordial yellow-blue system is
  • 9. transmitted on an autosomal gene, whereas red-green sensitivity is transmitted on the X chromosome (Mollon, 1986; Nathans, Thomas, & Hogness, 1986). Males, having one X chromosome--and so only one set of red-green system genes--are more likely than females to be color deficient (Mollon, 1986). In contrast, women are more likely than men to have evolved a fourth retinal photopigment that permits even greater differentiation of colors (Ja meson, Highnote, & Wasserman, 2001), consistent with the observed female advantage in sex-dimorphic color behavior (e.g., Bornstein, 1985). In humans (Morgan, Adam, & Mollon, 1992) and in nonhuman primates (Shyue et al., 1995), dichromats (who are more frequently males) are better able to detect texture and color-camouflaged objects. These empirical findings have suggested color-blindness may be adaptive for detecting and evading predation (Shyue et al., 1995). The genetic basis of color vision, therefore, is consistent with the speculation that color vision and, in particular the ability to discriminate red wavelengths, may have a greater adaptive significance for foragers (i.e., females) than for resource protectors (i.e., males) and so contribute to contemporary visual biases and object preferences. The recent finding that sex-dimorphic object preferences appear to exist in a nonhuman primate species (Alexander & Hines, 2002), suggests that, like color vision, sex-dimorphic object preferences appear to hav e arisen early in human evolution, prior to the emergence of a distinct hominid lineage. CONCLUSIONS There is increasing evidence that the brain has evolved specialized recognition systems for categories that have adaptive significance, such as emotional expressions and facial identity (for discussion, see Duchaine, Cosmides, & Tooby, 2001). In view of the evidence summarized above, it seems possible that males and females have also evolved specialized visual biases that optimize the development of sex-dimorphic behaviors with adaptive significance. The adaptive significance of spatial abilities consistent with hunting for males suggests that the male visual system (and in particular the M-cell pathway) is highly sensitive or responsive to objects that provide experience with tracking spatial movements of objects. This novel hypothesis is consistent with the proposal that toys, such as balls or cars, are more interesting to males than to females because they elicit motion (e.g., Eisenberg et al., 1982). If the female visual system (and in particular the P-cell pathway) has evolved to better forage for food or promote caretaking of infants, then female infants may be biologically prepared to be highly sensitive or responsive to object features--in particular color. Girls' preferences for dolls
  • 10. and warm colors (e.g., Iijima, Arisaka, Minamoto, & Arai, 2001) and a female advantage in facial expression processing (McClure, 2000) are all consistent with this possibility. This theory of sex-typed toy preferences predicts that parametric manipulation of those variables associated with the processing efficiencies of the different visual pathways (e.g., texture, spatial frequency, movement) will produce sex-specific effects on the visual preferences of infants and the toy preferences of older children. Further, given that infants appear to use perceptual features, such as vocal pitch (Miller, Younger, & Morse, 1982) to categorize males and females, it may be useful to consider whether the early development of color vision in infancy (Bornstein, Kessen, & Weiskopf, 1976; Teller, 1998) also provides information that contributes to gender category knowledge-- and whether this information is more salient to girls than to boys. Moreover, if aromatized androgens influence visual processing pathway development in humans, then androgenized girls compared to typically developing girls may show more masculinized patterns of visual development (e.g., later color naming, poorer object discrim ination, visual preferences for mechanical movement). Recent findings that androgenized girls show in free drawings more of the perceptual features associated with boys' drawings (i.e., attention to object movement and location) and fewer of the perceptual features associated with girls' drawings (i.e., attention to form and color; Iijima et al., 2001) are consistent with this possibility. Similarly, atypical toy preferences are an early feature of the atypical development of sex-dimorphic behavior (e.g., gender identity dysphoria, adult homosexual orientation; Bailey & Zucker, 1995; Zucker & Bradley, 1995), suggesting the gender-typical early organization of the visual processing pathways may be altered--perhaps by hormone effects during early postnatal development or by experiences with gender-linked objects during early infancy. If so, then male children with gender identity disorder, for example, may show feminized patterns of visual development (e.g., earlier color naming, greater color discrimination, b etter face processing). Whereas the sexual differentiation of the periphery (i.e., genitals) may be a primary determinant of gender socialization, early preferences for object characteristics may be an empirical window to a sex-typed "temperament," a product of the sexual differentiation of the central nervous system that evolved to predispose an interest in stimuli that promote the acquisition of a gender identity and gender role.
  • 11. Evolutionary psychology holds that an individual processes and experiences the external world as constrained by the survival and reproduction of the species (Bjorklund & Pellegrini, 2000). Accordingly, a transactional relation between a maturing individual and a changing environment is the formative force behind our developing cognitive strategies and abilities. Evolutionary theory is a challenge to understand the complex interplay between nature and culture, in the context of a more distal determinant of behavior, namely, natural selection. From this perspective, it seems that an association between toy preferences and gender role behavior may be mediated by sex differences in visual processing that evolved from the social roles of early males and females and are organized by hormones in perinatal development. Although hormones may organize structures that predispose an interest in object features, the general bidirectional theory of brain structure and brain function (Johnson & Morton, 1991) predicts that g ender socialization provides the required experiences that direct the sex-dimorphic specialization of the two visual processing streams. Thus, in view of the evolution of the phylogenetically older yellow--blue opponent system (Nathan, 1999) and the X-linked green--red opponent system (Mollon, 1986; Nathans et al., 1986), it may be more than a trivial coincidence that in our current culture we assign blue to boys and pink to girls. ACKNOWLEDGMENTS I thank Mark G. Packard and Bradley S. Peterson for helpful comments on an earlier version of the paper. Received December 4, 2001; revisions received April 8, 2002, and May 21, 2002; accepted May 21, 2002 REFERENCES Alexander, G. M., & Hines, M. (1994). Gender labels and play styles: Their relative contribution to children's selection of playmates. Child Development, 65, 869-879. Alexander, G. M., & Hines, M. (2002). Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabacus). Evolution and Human Behavior, 23, 467-469. Alexander, G. M., Packard, M. G., & Peterson, B. S. (2002). Sex and spatial position effects on object location memory following intentional learning of object identities. Neuropsychologia, 40, 1516-1522. Bachevalier, J., & Hagger, C. (1991). Sex differences in the development of learning abilities in primates. Psychoneuroendocrinology, 16, 177-188.
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  • 19. Brain. Contributors: Gerianne M. Alexander - author. JournalTitle: Archives of SexualBehavior. Volume: 32. Issue: 1. Publication Year: 2003. Page Number: 7+. COPYRIGHT 2003 Plenum Publishing Corporation; COPYRIGHT 2003 Gale Group