1.0 IntroductionSex differences in the nervous system arefound throughout the animal kingdom (Forger and de Vries, 2010). Sexual dimorphismcan be described as the differences in appearance between males and females ofthe same species, which goes beyond the differences in their sexual organs. Thedegree of sexual dimorphism found in mammals ranges from species in whichfemales are larger than males, to those in which males are much larger thanfemales and possess striking secondary sexual characteristics which femaleslack (Ralls, 1977).
In this paper, we are interested in the sexual dimorphismof mammal’s brains and how it can have an effect on certain behavioursdisplayed by males and females, specifically behaviours during copulation,maternal and paternal behaviours, and the hormones that influence theseparticular behaviours. In the past, numerous magnetic resonance imaging (MRI) studies have addressed thequestion of morphological differences of the brain of men and women, reportingconflicting results regarding brain size and the ratio of grey and white matter(Menzleret al., 2011). Thus,the relationship between sex differences in the brain and human behaviour is asubject of controversy in psychology and society at large (Fine, 2011).
To beable to elaborate on this topic, we first need to understand sexualdifferentiation and the process of developing into a male or female, from anundifferentiated zygote. 2.0Sexual Differentiation – DevelopmentSexrefers to the biological distinction between males and females. Hence, to beassigned as a female or male several factors are used to determine thebiological sex of an individual;chromosomes (XX for female, XY for male), gonads, hormones, internal sex organsand external genitalia (Knoxand Schacht, 2016). It’s stated that, the leading mechanism for sexualdifferentiation in mammalian species consists of a specific gene on the Ychromosome that triggers testis development in males. Hormones produced fromthe testes, mainly testosterone, then circulate throughout the body, differentiatingthe periphery and brain in a male direction (Forgerand de Vries, 2010). Most testosterone developmental effects on malebrain are actually via oestrogen which is a major driver of male braindifferentiation. In female mammalian species, a lack ofthis early exposure to the high levels of testosterone, due to the absence oftestes, allows development of default feminized characteristics (Matsuda, Mori and Kawata,2012).
This can be described as aprimary organisational effect, as generally organisational effects of hormonesoccur at development. 2.1Sexual Differentiation – Post-PubertyPost-puberty,hormones have activational effects.
Theyinitiate sex-specific behaviours through actions via male and female body and brain.It was found that, new cells, includingneurons, arise in many brain regions during puberty in both male and female rats.Sex differences found in pubertal addition of these new cells correspond withsexual dimorphisms found in adults: “for each region, the sex that gains morecells during puberty has a larger volume in adulthood”. Removing gonadalhormones before puberty eradicates these sex differences, indicating thatgonadal steroids are the reason for the addition of new cells during puberty to maintain andaccentuate sexual dimorphisms in the adult brain (Ahmed et al., 2008). However,the broad hypothesis for mammalian species indicates thatchromosomal sex genes are responsible for gonadal differentiation and thatgonad specific hormones initiate sex specific brain organization.
In recentyears, this principle has been challenged with evidence suggesting that somesexually dimorphic brain development occurs independently of peripheral signals(Schlinger, Soma andLondon, 2001). Although it is clear that gonadal hormonescan have dramatic long-lasting effects on the brain during development, it isnoted that even after puberty and into adulthood gonadal steroids can modifyneuronal structure and even have permanent effects on certain reproductivefunctions (Gorski,1986).2.2Sexual Differentiation – The BrainStudiesof brain regulation and human behaviour require measurement of structuralvariables, and this has been done predominantly by post-mortem studies (Gur et al., 1991). Sexualdifferentiation of the brain can be considered as a process during whicheffects of sex steroid hormones secreted during early development is maintainedinto adulthood (Matsuda,Mori and Kawata, 2012). Sexualdimorphisms between males and females are apparent in several brain areas,including the preoptic area (POA), bed nucleus of the stria terminalis (BNST)and hypothalamus (McCarthyet al., 2009).
A report of thefirst meta-analysis of typical sex differences on global brain volume foundthat, males on average have much larger volumes and higher tissue densities inthe left amygdala, hippocampus, insular cortex, and cerebellum. However, femalestypically have higher densities in the left and right frontal poles (Ruigrok et al., 2014). However, these findingsconflict with other articles written, and so the relationship between sexdifferences in the brain and human behaviour is a subject of controversy inpsychology and society at large (Fine, 2011).3.0 Sex Behaviour – FemalesThe display of copulatory behavioursusually requires the existence of a mate and is, therefore, preceded by asearch for and approach to a prospective mate of the opposite sex. Theintensity of approach behaviours is determined by a process labelled “sexualincentive motivation” (Spiteri et al., 2010).
Sexual motivation is typically influenced by hormones suchas testosteronein males, oestrogenand progesterone in females, and oxytocin in both sexes. In many mammalian species, these sexhormones control the ability to engage in sexual behaviours, and thesebehaviours can be described as sexually dimorphic. Young stated that, most investigations of cyclicreproductive activity in female mammals have been more interested in thefunctional basis of the morphological changes and less interested in ananalysis of the factors underlying the parallel changes in behaviour (Young,1941). During his studies on mating behaviour in female mammals he found thatwith white rats, movements during copulation are often fast-paced and darting,with hops accompanied by a shaking of the ears or the entire body.
Females donot run away from the male, except that following a moment of smelling orlicking by the male, she runs forward a short distance and stops where thefemale is then overtaken and caught in the copulatory clasp by the male. Whenmounted by the male or fingered on the hindermost part of the back and aroundthe base of the tail a lordosis is shown (Young, 1941). The female rats controlthe pacing of mating through three phases before lordosis; approach,orientation and runaway. Similar behaviour was recorded for other mammals, fromwild rats, to cows, and further. The females appear to show a more submissivebehavioural attitude when it comes to mating with a male, possibly due to thedifferent hormones released that influence sexual behaviour. This theory isbacked up as certain findings suggest that the gonadal hormones can influencesubmissive behaviour in female Syrian hamsters (Faruzziet al., 2005).
3.1Sex Behaviour – MalesMalemating competition is largely regarded to account for sexual dimorphisms inbody size (Mitani, Gros-Louis and Richards,1996). Previously it was concludedthat, because male mammals often compete more aggressively among themselves foraccess to mates than females do, sexual selection is assumed to be a farstronger force among males, than females (Darwin, 1871). Sexual selection canbe divided into two processes: intrasexual selection, which involves members of the same sex within a particularspecies competing with each other in order to gain opportunities to mate withothers, andintersexual or epigamic selection, in which members of one sex choose to mate withmembers of the opposite sex (Ralls, 1977). However, most research on sexual selection in mammals has highlightedthe importance of intrasexual selection, for example, “among mammals therole of aggressive male behaviour tends to be more important than that offemale choice” (Brown 1975). Furthermore, testosterone is the key male gonadal steroidwhich influences male mating behaviour. The magnocellular medial preopticnucleus (MPN mag), a subdivision of the medial preoptic area (MPOA), playsa critical role in the regulation of copulation in the male Syrianhamster; in part by facilitating the effects of gonadal steroids (Brague et al., 2018).
It was also found that, raisedlevels of gonadal androgens are often required for the expression of male-specificbehavioural and morphological traits in all classes of vertebrates (Golinski et al., 2014).These behaviours can be described as more masculine, as mounting and, onoccasion, severe aggression can be seen being displayed. 4.0Hormones and Behaviour (Maternal and Paternal)Parental behaviour is brought about by acombination of internal processes and external factors that ensure the parentstake care of the young, contributing to their survival by providing food,shelter, warmth, protection, and appropriate stimulation.
In mammalian species,lactating females are mostly responsible for providing all the care, however, malesand other family members can also contribute to the care of the offspring insome cases (Olazábal et al., 2013). Although studies of mammalianmaternal behaviour are abundant, there have been very few reports on theassessment of paternal care (Elwood, 1975). Testosterone is known to promote an extensive array of behavioursassociated with reproduction in males, including intermale competition, matingbehaviour and courtship behaviour (Adkins-Regan 1998). In a number of mammalianspecies, male testosterone levels decline after the birth of offspring (Brownet al.
1995). These findings would suggest that testosterone has a negativeeffect on paternal behaviours, however it previously found that testosteronepromotes paternal behaviour in the California mouse (Peromyscus californi) (Elwood, 1975) as behaviours such as lickingand sniffing the pups were seen, accompanied with an increased testosteronelevel. Due to these discrepancies, there is still much we don’t know about thehormones which regulate and facilitate this paternal behaviour. However, it was concluded that, the mostconsistent evidence for the involvement of hormones in mammalian paternalbehaviour is for prolactin, which was found in species such as the goldenhamster (Mesocricetus auratus), mouse(Mus musculus), and rabbit (NewZealand White) (Wynne-Edwards, 2001). This canalso be seen in human fathers (Fig.1).
Figure 1. Mean (± SE) levels of Oxytocin and Prolactin in first-time human fathers in the second and six month following birth of the child. (Sourced from Gordon et al., 2010) Furthermore, current research into thebehavioural endocrinology of male parental behaviour is testing the hypothesisthat paternal and maternal behaviour are homologous at a neural and anendocrine level (Wynne-Edwards and Reburn, 2000). If homologous, then the samehormones would act at the same neural sites to enable the expression of thesame parental behaviours in both males and females (Wynne-Edwards, 2001). This is a valid statement as evidencefor this could be in the fact that males and females have almost all the sameDNA, apart from a number of genes on the Y chromosome, thus, sex differences in behaviourshould come from differential gene expression, rather than structuraldimorphism (Kelley, 1988). Onthe other hand, as previously stated, there are numerous reports anddiscussions about mammalian maternal behaviour. In nonhuman primatesand humans, similar to other mammals, hormones are not strictly necessary forthe expression of maternal behaviour, but nevertheless influence variation inmaternal responsiveness and parental behaviour both within and between individuals(Saltzman and Maestripieri, 2011).
Whenconsidering the neuroendocrinology of primate maternal behaviour, initialevidence indicates that oxytocin and other endogenous opioids affect maternalattachment to infants, this includes care, contact, grooming, and responses toseparation. Serotonin in the brain affects anxiety and impulsivity, which mayaffect maternal behaviours such as infant retrieval or rejection (Saltzman and Maestripieri, 2011). It is believed that, further studies on maternal and paternal motivationwill continue to add complexity to the system, and contribute to our overall understandingof the mechanisms that regulate these behaviours, as well as the processesunderlying maladaptive behaviours and psychopathologies (Olazábal et al., 2013).
5.0ConclusionTo conclude,although most sexual dimorphism appears after gonadal differentiation, some canoccur at earlier stages in development (Kimura and Matsuyama, 2012). Furthermore, the mammalianbrain is not hugely dimorphic between sexes, although differences clearly existfor example, in the preoptic area, left amygdala and hippocampus, as well as differences seenin brain size and the abundance of grey and white matter. However, they are notextensive in most species. Most differences are seen in the behavioursdisplayed between sexes. These behaviours can be described as dimorphic betweensexes and generally play a role in activating, modulating, or inhibitingcertain aspects of maternal or paternal behaviours in mammalian species. Femalelordosis and male mounting or aggression during copulation are also sexuallydimorphic behaviours that can be influenced by gonadal hormones testosteroneand oestrogen.
Further studies are however required to gain a more extensivelook at the mammalian brain and neuroendocrinology of both maternal andpaternal behavioural patterns and how other environmental or physiologicalfactors may affect these. ReferencesAdkins-Regan, E. (1998) Hormonal mechanisms ofmate choice. Am. Zool. 38, pp166-178.Ahmed,E.
, Zehr, J., Schulz, K., Lorenz, B., DonCarlos, L. and Sisk, C.
(2008).Pubertal hormones modulate the addition of new cells to sexually dimorphicbrain regions. Nature Neuroscience. 11(9), pp995-997.Brague,J., Zinn, C.
, Granot, D., Feathers, C. and Swann, J. (2018). TrkB is necessaryfor male copulatory behavior in the Syrian Hamster ( Mesocricetus auratus).
Hormones and Behavior. 97, pp162-169.Brown, J. L. (1975). The evolution of behavior.Norton, New York. pp160.
Brown,R., Murdoch, T., Murphy, P. and Moger, W.
(1995). Hormonal Responses of MaleGerbils to Stimuli from Their Mate and Pups. Hormones and Behavior. 29(4), pp474-491.Darwin, C. R. (1871).
The descent of man andselec tion in relation to sex. John Murray, London, United Kingdom, pp475.Elwood,R. (1975). Paternal and maternal behaviour in the Mongolian gerbil. AnimalBehaviour, 23, pp766-772.Faruzzi,A.
, Solomon, M., Demas, G. and Huhman, K.
(2005). Gonadal hormones modulate thedisplay of submissive behavior in socially defeated female Syrianhamsters. Hormones and Behavior. 47(5), pp569-575.
Fine,C. (2011). Delusions of gender: how our minds, society, and neurosexism createdifference. Choice Reviews Online. 48(6), pp48.Forger,N. and de Vries, G.
(2010). Cell death and sexual differentiation of behaviour:worms, flies, and mammals. Current Opinion in Neurobiology. 20(6),pp776-783.Golinski,A., Kubi?ka, L., John-Alder, H.
and Kratochvíl, L. (2014). Elevatedtestosterone is required for male copulatory behavior and aggression inMadagascar ground gecko (Paroedura picta). General and ComparativeEndocrinology, 205, pp133-141.Gordon,I., Zagoory-Sharon, O., Leckman, J.
and Feldman, R. (2010). Prolactin,Oxytocin, and the development of paternal behavior across the first six monthsof fatherhood. Hormones and Behavior, 58(3), pp513-518.
Gorski,R. (1986). Sexual differentiation of the brain: a model for drug-inducedalterations of the reproductive system. Environmental HealthPerspectives.
70, pp163-175.Gur,R., Mozley, P., Resnick, S., Gottlieb, G., Kohn, M., Zimmerman, R.
, Herman, G.,Atlas, S., Grossman, R. and Berretta, D. (1991). Gender differences in ageeffect on brain atrophy measured by magnetic resonance imaging. Proceedingsof the National Academy of Science., 88(7), pp2845-2849.
Kelley, D. B. (1988). Sexually dimorphicbehaviours. Review Neuroscience.
11,pp225–251.Kimura,K. and Matsuyama, S. (2012). Sexual Dimorphism during Early EmbryonicDevelopment in Mammals. Journal of Mammalian Ova Research, 29(3),pp103-112.Knox,D.
and Schacht, C. (2016). Choices in relationships. 1st ed.Boston, Massachusetts: Cengage Learning, p.33.Matsuda,K., Mori, H.
and Kawata, M. (2012). Epigenetic mechanisms are involved insexual differentiation of the brain. Reviews in Endocrine and MetabolicDisorders, 13(3), pp163-171.
McCarthy,M., Auger a., Bale T., De Vries G., Dunn G., ForgerN., Murray E., Nugent B.
, Schwarz J., Wilson M. (2009) The epigenetics of sex differences in the brain. Journal of Neruoscience. 29(41).
Menzler,K., Belke, M., Wehrmann, E., Krakow, K., Lengler, U., Jansen, A., Hamer, H.
,Oertel, W., Rosenow, F. and Knake, S. (2011). Men and women are different:Diffusion tensor imaging reveals sexual dimorphism in the microstructure of thethalamus, corpus callosum and cingulum. NeuroImage.
54(4),pp2557-2562.Mitani,J., Gros-Louis, J. and Richards, A.
(1996). Sexual Dimorphism, the OperationalSex Ratio, and the Intensity of Male Competition in Polygynous Primates. TheAmerican Naturalist, 147(6), pp966-980.Olazábal,D.
, Pereira, M., Agrati, D., Ferreira, A., Fleming, A., González-Mariscal, G.
,Lévy, F., Lucion, A., Morrell, J., Numan, M.
and Uriarte, N. (2013). New theoreticaland experimental approaches on maternal motivation in mammals.
Neuroscience& Biobehavioral Reviews, 37(8), pp1860-1874.Ralls,K. (1977). Sexual Dimorphism in Mammals: Avian Models and UnansweredQuestions. The American Naturalist, 111(981), pp917-938.Ruigrok,A., Salimi-Khorshidi, G.
, Lai, M., Baron-Cohen, S., Lombardo, M., Tait, R. andSuckling, J. (2014). A meta-analysis of sex differences in human brainstructure.
Neuroscience & Biobehavioral Reviews. 39, pp34-50.Saltzman,W.
and Maestripieri, D. (2011). The neuroendocrinology of primate maternalbehavior.
Progress in Neuro-Psychopharmacology and BiologicalPsychiatry, 35(5), pp1192-1204.Schlinger,B., Soma, K. and London, S. (2001). Neurosteroids and brain sexualdifferentiation.
Trends in Neurosciences. 24(8), pp429-431.Spiteri,T., Musatov, S., Ogawa, S., Ribeiro, A.
, Pfaff, D. and Ågmo, A. (2010).
Estrogen-Induced Sexual Incentive Motivation, Proceptivity and ReceptivityDepend on a Functional Estrogen Receptor ? in the Ventromedial Nucleus of theHypothalamus but Not in the Amygdala. Neuroendocrinology. 91(2),pp142-154.Wynne-Edwards,K. (2001).
Hormonal Changes in Mammalian Fathers. Hormones and Behavior,40(2), pp.39-145.Wynne-Edwards, K.
, and Reburn, C. (2000).Behavioural endocrinology of mammalian fatherhood. Trends Ecol. Evol. 15(1), pp464– 468.Young, W.
(1941). Observations and Experiments onMating Behavior in Female Mammals. The Quarterly Review of Biology.16(2), pp135