GENDtr,R AND SOCItr,TY
EssaysBased on Herbert Spencer LecturesGiven in the (Jniversitv of Oxford.
Edited by COLIN BLAKEMORE WaynfleteProfessor of Physiology and Fellow of Magdalen College. SUSAN IVERSEN Professorof Experimental Psychologyand Fellow of Magdalen College.
OXTORD UNIVERSITY PRESS OX'FORD IJNIVERSITY PRESS Grcat ClarendonStrce t. Oxford ox: 6ot' Oxford UniversityPress is a departmentof the Universityol Oxford. It furthersthe University'sobjective of excellencein rescarch.scholarship. and educationby publishingworldwide in CONTENTS Oxford Ncw York Athens Auckland Bangkok Bogotii BuenosAires Calcutta CapeTown Chennai Dar es SalaamDelhi FlorenceHong Kong Istanbul Karachi KualaLumpur Madrid MclbourneMexico Citv Munrbai 'laipci 'lbkyo 'lbrottlo Nairobi I)arisSito l)itulo Singapore Warsaw and associatedcompanies in Berlin lbadan List of Figures \rl Oxlord is a registered trademark of Oxford UniversityPrcss in the UK andcertain other countries Vi Publishedin the UnitedStates Lisr of Tables by Oxford UniversityPress Inc., New York O the SeveralContributors 2ooo List of Contributors vll The moral rightsof the authorhave been asser(cd Databaseright Oxford University Press(maker) First publishedzooo Sex and Molecular Biology All rightsreserved. No part of thispublication may be reproduced, PETER N. GOODFELLOW storedin a retrievalsystem. or transmitted.in any form or by anymeans, rvithoutthe prior permissionin writingof Oxford UnivcrsityPre ss, or asexpressly permitted by law,or undcrterms agrecd with the appropriatc Gender and Population r3 reprographicsrights organizations.Enquiries concerning reproduction outsidethe scopeof the aboveshould be sentto the RightsDepartment. SUSAN COTTS WATKINS Oxford Univcrsity Prcss,at the addressabove You mustnot circulatelhis book in anyother binding ()r cover and you mustimposc the samecondition on any acquiror SexualDifferentiation and CognitiveFunction LUCIA JACOBS BritishLibrary Cataloguing in PublicationData Data available Libraryof CongressCataloging in PublicationData A Little Learning:Womenand (lntellectual)Work 97 Genderand society: the HerbertSpencer lectures / editedby Colin Blakemore, MICHELE LE DOEUFF SusanIversen. Includesbibliographical references and index. t. Sexrole. z. Sexdifferences. 3, Women-Socialconditions. l. Blakemore,Colin. Il. Iversen.Susan D.. 1940- VictimsNo Longer:Feminismand the Reformof HQro75 .G.q6r9:ooo 3o5.3-dczr gg-o'7t9"+ CriminalLaw r r'l ISBN o-t9-1129792 Index 20t J SexualDifferentiation and CognitiveFunction LUCIA JACOBS ,l In 1588,Michel de Montaigne concluded, say that male and female are cast in the same mold: save for education and customthe difference betweenthem is not great' [62].If Montaigne could be asked about the relative prop".ii., of men and women in the area not only of morphologv and outward behaviour,but also of cognition I suspecthe *,oulcl give the sameanswer, perhaps more adamantly.yet il is an interestingquestion: how do the sexesdiffer in their percep- tion and processingof information about their external world? And if such differencesexist, do they develop 'education due to and custom',or are cognitivesex diffeiences a consequenceof sexual differentiation? And if such dif- ferences exist, can we supposethat they are functional (i.e. do they occur in other speciesand have they arisenthrough processesof natural selection?). Questions about sex, gender, and cognitive ability are topics of intrinsic and universalinterest, a field of enquirv which hasgenerated tens of thousandsof schorarryarticrei. It is also a field mined with potential political dangersand divisions,and one into which biology vintures at great risk. The firm establishmentof the principles and ramificationsof I would like to thankKim Beenran,Marc Breedrove,John Dark. Kare onstort. Presro'' Margo,wilson, and carol worrhman for helpfuldiscussion otllt*.lf lne ldeas drscussedhere. I rvould also like t;r acknorvledgithe financial supportof the Universityof Californiaat Berkelev. )J Lucia Jacobs Sexualdifferentiation snd cogrtitivefunctiort sexualdifferences, unrelated to culturalcontext, is an impor- functionalexplanation for this sexualdimorphism is that in tant goal,but it lieson the far sideof treacherousintellectual polygynousspecies, males compete amongst themselves for terrain.But we can,at thisjuncture of the expedition,find u..Lrt to females,and thereforerequire proportionately placesto setour feetthat will not leadto disaster.generali- largerbody sizesthan femalesin order to reproduce'In the zationsthat, presumptuousthough they may be, biologists red deer(Cervus elaphtts), for example'larger stags are more feel will survivetheir time and their cultural context.For successfulin defendinga haremof hindsand hencea stag's example,I would arguethat it is a landscapethat must be bodysize is directlyproportional to hisreproductive success understoodwithin a historicalframework. which. to a biolo- Itz]. gist, is the frameworkof evolutionby naturalselection. Despitethe controversy, all would agreethat we haveat least threegood landmarks on which to baseour map.These are: Sexual selection and song first,that in all vertebratespecies, male and femalecognitive abilitiesand brains are more alikethan different;second, that Sexual dimorphisms in body size or antler weight mav suchdifferences can arise through the actionof hormoneson have little to do with cognition,but illustratethe adaptive neuraldevelopment;and third, that the internal environment significanceof sex differences.The boldest and most easilv of the hormonalmilieu is influencedboth by the geneticsof explainedexample of a cognitivesex difference is alsofounc sexdetermination and by the externalenvironment. Hence, in the context of malescompeting for fenralematcs.llris is sexdifferences in the brainand in cognitiveabilities can be the ability of songbirds,also known as passerinebirds. to stronglyinfluenced by the combinedactions of the environ- learn their species-specificsong. Passerinebirds contprise mentand an individual'sgenetic make-up. over half of all bird speciesin the world. and in manv s;recics Using theselandmarks, each discipline constructs its own males must learn to sing [57].These song-learningspecies mapof thisterrain, each perhaps with a distinctivedistortion, show much variability in the timing and tutoring of song: 'View much as SaulSteinberg's 1975 of the World from 9th some specieslearn only at one time period during develop- Avenue'is a tcpclcgicallycorrect but geometricallydistorted ment (criticalperiod or age-limitedlearners) and somelearn representationof the world from the point of view of a New throughout life (open-endedlearners), some learn from a Yorker [Z:]. My route throughthis terrain is basedon the parentand somelearn from surroundingadults. Yet acrossall map of a cognitivepsychologist trained in the pracriceof song learning species,there is a sex difference:males sing ethologyand the rheoryof evolution.I beginwith the bio- more complexsongs than females.Although it is true that in logicalunderpinnings: the distributionof cognitivesex dif- some speciesfemales and malessing duets.where eachpart ferencesin speciesother than our own, and the causesand is of equal complexity,in no speciesdo femaleslearn to sing consequencesof this patternin other species. more complexsongs than males[76]. The puzzleunderlying cognitive sex differences is why sucl, The function of this distinctsex differenceis clear:males a fundamentaltrait as cognitionshould differ oetweenthe require learned song to attract fen:ale mates and to compete sexes.Yet the samecan be saidof even more fundamental againstmale rivals.The ability to learn song is thus subject traits,such as body size.For example,in many polygynous to sexual selection,the selectivepressure rvhich result from mammals.despite similarities in ecologicalniche between competition anong individualsof the same sex h6]. Song malesand females,males are larger than females[4]. The learningability lendsan advantageboth in territory disputes 56 57 Lucia Jacobs Sexualdifferentiation and cognitivcfitnctiort and in female preference:in open-endedlearners, males with its neural basis. The different hormonal milieu of males large song repertoires attract more females.A larg,3rspsl- and females produce sex differences throughout the fine toire is also necessaryfor effective territory defence,because structure of these brain areas (e.g. the volume of brain in many species,the mode of competition among males is regions,the number of neurons,the size of neuronal cell their ability to match the songsof their rivals.Neighbouring bodies, the length of dendrites, and the distribution of males mimic each other's repertoire, song for song, appar- receptors for steroid hormones). Yet if hatchling females ently an efficient method by which they size up each other's are injectedwith the steroidhormone oestrogen,the volume repertoire[8]. Sincerepertoire often increaseswith age,this of song nuclei areas are increasedvia reduced neuronal may providethe listeningbird with someestimate of the com- death and such females rvill both sing and learn sonq petitive characteristicsof his neighbour. syllablesfrom a tutor. If these femalescontinue to receive For these and other reasons,birdsong is considereda sex- male-appropriate steroid hormones as an adult, she rvill ually selectedtrait, with advantageaccruing to those who can develop further changesin structure, all with the effect of learn more complex song than rivals. And since in most producinga femalebrain whosesong nuclei are increasingly species,it is the males who compete more strongly than similar to those of males [6]. femalesfor mating opportunities,it is the maleswho receive Although birdsong is a clear example of a cognitive sex dif- the brunt of the sexualselection for song learning,And hence ferencein vertebratesand an excellentsystem for the studv the clear dimorphismin learningability. of their development,it also has the drawback of the special How this dimorphismdevelops and by what precisemech- case;no other species,avian or otherwise,learn songs.But in anismthis occurs,is itselfa thriving scientificdiscipline [6]. In its generaloutlines, it can be thought of as a templateto brief,however, it is a storyof hormonalenvironments, created searchfor other casesof sexdifferences, u,ith these attributes. by the hormone output of the fetal and perinatal gonad.If it shows enhanced development in the sex experiencirrg the brain tissueof the developingsongbird, such as the well- greater sexual selection,it is shaped by the hormonal en- studiedcanary or zebra finch,experiences high levelsof the vironment during a critical perinatal period, and with the hormone that normally emanates from the male gonad, degreeof neuraldimorphism is directlyrelated to the deqrcc during the critical period immediately after hatching,this of cognitive dimorphism.These attributes are present only in leadsto the structuralenhancement of certainnuclei, known one exampleof cognitivefunction in mammalsand this is in as the song nuclei.In the zebra finch,where femalesdo not the realmoi spatialcognition. sing at all, this producesa striking difference in morphology between male and female brains.The male brain contains a series of interconnected nuclei, the song nuclei, which are Sextral selection and space necessaryto learn and produce song and which are smaller or absentin the female brain.The detailed circuitry and func- Spatial cognition is usually defined to include assortedper- tions of these nuclei is outside the province of this essay;the ceptual and mnemonic abilities,such as the ability to perceive obvious conclusion,horvever, is that both learning ability and and locate visual objects in space and the ability to create its underlying brain structure are sexually dimorphic [6]. map-like internal representationsof the environment. Thus 'spatial Hence, here is an everyday occurrence of a sexually cognition'includes both simple and complexspatial dimorphic learning ability, with underlying dimorphism in processing. 58 59 Lucia Jacobs Sexual differentiation and cognitive futtction Male and female laboratory rats,the domesticstrain of the the far-off landmarks and would therefore not change his wild Norwegian rat (Rattusnorvegicus), show striking differ- searchstrategy at all. If the objectsare not just rotated but encesin what they remember from exploring new environ- are mixed up, so that different objects are exchangedwith ments.These differencesemerge when the rats are asked to eachother, then femalessuddenly can no longerfind the bait use visual landmarks to return to the food they had found in the maze',she now makes as many niistakesas the males earlier,such as location of bait in a maze [92].Fiow well males surroundedby the curtain. and females are able to find the bait depends on how the What is the mechanismby which this remarkablecognitive visual appearanceof the test room has been changed.If the sex differencearises? Once again,it is the early hormonal maze is surroundedby a white curtain,so that the shapeof environment[qz]. If a rat, regardlessof sex.experienccs its the spaceis changed,males make many more mistakes.It is first week of life in the presenceof a certain level of repro- as if thel' ^'^ using the shapeof the room as a compass,to ductive hormone (oestrogen)in its blood, either produced tell them where they are.Thus, if the room is rectangularwith naturally by male testesor artificiallyby injection.then that a door at one end, the male rat carr place himself in this individual,as an adult, will pay attentionto the 'contpass simple map, and remember,for example,that he has already marks' or distant landmarks, and it will make many more 'door looked for bait at the end'. Or he can use several of errors in the curtained maze.If a rat does not experiencethis these far-off landmarks,such as the door, or the corners of levelof oestrogen,either becauseits brain producesa certain the room, at the same time, to define (or triangulate) a protein which mops up excessoestrogen. as happens in specificpoint in the room, such as the arm of a maze.Thus, if normally developingfemales, or becausedisease or experi- the male is paying most of his attention to these types of far- mentalintervention prevent the testesfrom producingtestos- off landmarks, he will be badly handicapped if these outer terone (which is then convertedto oestrogen.the necessarv landmarksare suddenlycovered by a curtain.This is exactly form of hornrone),then th. rat will pay attcntionboth to what happens:he starts looking in the wrong places,revisit- distant corners and closer objects,as describedfor nornral ing placeswhere he has already eaten the bait, for example, females. until the curtain is once again removed.Then he can once This scenariois almost identical to that describedfor the again solve the maze with almost no errors. developmentof birdsong.This is perhapssurprising that such Female rats behave quite differently.They also appear to different learningabilities, song and space.would developin learn the corners of the room becausethey also make more such similar ways:after birth or hatching.and in response mistakeswhen the curtains are used. But they are not as simply to the hormonesproduced by the neonatalgonad. We affected as the males.This is becausefemales have also paid can only speculatewhy this is so;why perhapssophisticated attention to the location of objects that are closer to the learningabilities only appearlate in brain development.after maze,such as items on the table or glued to the wall. The the staplesof sensoryperception. motor coordination.learn- femalesnot only usethe compassand triangulation technique ing, and memory of sensoryinformation have alreadybeerr to define a place in space,but also remember the items that built. Perhaps,too, it is a good thing to have this tardy devel- were near that place,such as the box on the table that was opment of these structures,so that they develop not as a behind that arm of the maze. If these objects are rotated, closed genetic programme,but as one more flexible arrd females rotate their searchpattern, just as if the whole room responsiveto the environment. had been rotated.A male, however,would continue to use Moreover, if spatiallearning parallelsbird song learning. 6o 6r LuciaJacobs Se.rttaldifferentiotion ond cognitit'c.fturctirtrt thenit shouldalso be mediatedby a part of the brain that defendedspaces. This sexdifference in spaceuse arises from developsduring the critical postnatalperiod and that is different mating strategiesof males and females:fenlales responsiveto gonadalhormones during this time.These con- defendan arealarge enough to feedthemselves and their off- ditionsare met by one structure,the hippocampus.The hip- spring,while males spend their time searchingfor females pocampusis a largeforebrain structure with bothgeneral and receptiveto mating.Under this polygynouss)'stem. the dii- specificcognitive functions. Its generalfunction is the ability ferencein natural spatialmovements by malesand females to constructand remember conceptual relationships between is reflectedin similar differencesin spatiallearning. such as eventsfz7l. lt alsohas a specializedfunction to solveprob- mazeperformance.That this differenceis relatedto spaceuse lemsof s:^.'^l representations,such as the ability to mapand is suggestedby the further observationthat in monogamous constructnovel routes in the externalworld [67].Moreover, speciesof rodents,where malesand femalesuse territories of like songnuclei, the hippocampusmay be sexuallydimorphic the samesize. there are no sex differencesin the number of in sizein both birds [78] and mammals[42]. In laboratory errors made learningmazes [:2,:f]. rodents,the hippocampusis sexuallydimorphic, with a male Thus,sex differencesin behaviour are directly related to advantage,in cell number[9+], in the volumeof fibre tracts learning spatialinformation in nature.How could this explain [55],and in the volumeof the certaindendritic arbors [47J. why male laboratoryrats concentrateon the cornersof the And, just as in birdsongnuclei, these sex differencescan room? Perhapsit is becausemales specializein learningto be manipulatedby changingthe earlyhormonal environment find locationsquickly, by triangulatingtheir coordinatesfronr in which the hippocampusdevelops; females treated with distant objects.This is an extremely-efficientrvav to solve a testosteroneat birth show a masculinizedpattern of spatial mazewhich only requirs5a simplesolution. such as learning learning and hippocampalstructure [72]. Thus, both sex the location of a few bait locations.But this strategvvields differencesin spatial learningin the rodent and sex dif- little other information.Females. in contrast.may be learnirtq ferencesin the hippocampuscan be alteredwith hormones, their territoryin much greaterdetail. Hence. females appeaf althoughthe precisemechanism by whichhormones change to solvel"he maze more slowlyonly becausethev take in nrore the fate and structure of the hippocampusis not fully information than do males.Thus, if femaleslearn two t1'pes understood. of spatial information (e.g.both compassdirection and the While it is clearthat malebirds sing so that femaleswiil be individual features of different landmarks),their progress attractedto them,it is not at all clearwhy male rats should must be slower;theyare learningmore arrdhence learn ntore navigatebased on the shapeof a room; at least,when the slowly [93].Again, this makes good sehsein the real rvorld: questionis statedin that way.So we must insteadstep back female rodents rear litters by__theirown efforts. and should andask: what is the functionof navigation,under raturalcon- know their own territory well in order to forage more ditions?Why would malesand femalesdiffer in how they efficiently.ln contrast,for malesto increasetheir successas accomplishthis? The answerlies in the observationof space reproductivecitizens, they must travelfarther. encounter. and usein nature.Sex differences in mazenavigation have been court a greater number of females. demonstratedin severalspecies of wild rodents.In all of these The advantageof spatial navigation ability in males has species,males and femaleshave different patterns of natural been best demonstratedin field studies of the thirteen- spaceuse: males use large, undefended areas which encom- lined ground squirrel (Sperrnophilus tridecentlineatus).hl passthe territoriesof severalfemales, which live in small this species,females are receptivefor only one day per )/ear. 6z 63 LLtciaJacobs Se.vtuIdifJ-erentiation antl cogttitivefurtctittrr Malesarrive on a receptivefemale's territory and follow a havelarger testes and caninesthan malesfrom speciesrvhere queuingconvention;the first onesto arriveare alsothe first polygynyis lessextreme [+, t8]. onesto mate.A male'sability to find receptivefemales as Patternsof mate competition also predict the magnitude soon as possibleon their day of oestrusthus has a direct of sex differencesin the brain [43].The dimorphismof song greater finch (Poephila effecton a male'ssuccess [75]. nuclei, for example, is in the zebra Thus,like songbirds,rodents also show cognitivesex dif- guttata),where femalesdo not sing at all, than in the canarv ferences.The directionof the sexdifference is not fixed,but (Serinuscanarius),where females sing a simplesong.The sex variespredictably with mating system,and thesepatterns difference in song nuclei size is even smaller in the bay- predictsex differencesin the hippocampus,a major neural breastedwren (Thryothorus nigricapillus).rvhere nrated pairs substratefor spatial navigation.Finally, the sex-specific sing intricateduets, composed of two equallycomplex parts. spatialspecializations appear to be adaptivesolutions to the Hence the larger the sex differencein song complexity.the different spatialproblems faced by males and femalesof Iargerthe sex differencein song nuclei Ir6]. thesepolygamous species in nature. Sex differencesin hippocampal size also vary with natural Yet, comparedto the magnitudeof cognitiveand neural patternsof learningability and spaceuse. In contrastto poly- sexdifferences in songbirds,these differences are not great. gynous vole species,in the monogamouspine vole (fulicrottts In this sense,Montaigne was still correctin sayingthat even pinetorum), where a male, under natural conditions.uses for rodents,males and femalesare more alikethan different. the samesize territory as his mate.there is no sex difference in eitherspatial learning ability or hippocanrpalsize [:2.++] The samepattern is seenin the spaceuse patterns of birds:in Of mice and men the brood parasiticbrown-headed cowbird (Molorhrusnrer). femalescompete for suitablehost nestsin which to lay their For the animal shall not be measuredby man. In a world older and eggs.Because they must lay their unwelcome egg without more complete than ours they move finished and complete,giftec being detectedby the host,females must rememberboth the with extensionsof the senseswe have lost or never attained,living locationsof host nests and their hosts' laying scheduleto by voices rve shall never hear.They are not brethren, they are not executea successfulforay. In the North Anrerican cowbird. underlings;they are other nations,caught with ourselvesin the net this behaviouris correlatedwith a female advantagein hip- of life and time, fellow prisonersof the splendour and travail of the pocampalsize [78]. In Argentineancowbirds (M. I';onnriensis. earth. Henry Beston(r928) r] [r M. rufoaxillaris,M. badiLts),the degree to rvhich any species Yet even sovereignnations may obey the samenatural relieson brood parasitismdetermines the sizeand drrection laws.We aremammals, after all, and show typical mammalian of this female advantagein hippocampalsize: species where sexdifferences in bodysize. Sexual dimorphisms in structure the male and female searchfor host neststos,ether shou, a are common;in fact, wheneverone sex cannot maintain smallerfemale advantage [7r]. exclusiveaccess to another,the toolsof competition,such as Thus the degree of investment in structuresneeded to weapons.body size,even testes size, appear in more exag- competefor matesis correlatedwith the level of mate cont- geratedforms. The degreeof sexualselection determines petition.In primates,this can be predictedfrom the number both the trait and the degreeto which the trait is sexually of females to whom a male is able to maintain exclusive dimorphic.For example,highly polygynousmale primates access,and sexual dimorphism in body size in primates is 64 65 Lucia Jacobs Sexual differentiation and cognitive function directlyrelated to theratio of femalesper male in a socialunit Edward C.Tolmanhimself, who attempteda similarsynthesis Ir8].Because human polygyny is characterizedby a relatively on mice and men with his 1948 paper,'CognitiveMaps small number of women per polygynousgroup, sex differ- in Rats and Men'-'My argumentwill be briel cavalier,and encesin statureand other measuresshould be correspond- dogmatic.For I am not myself a clinician or social psy- inglysmall, at leastin comparisonto specieswhere the ratio chologist.What I am going to say must be considered. of availablefemales to availablemales is much smaller.In therefore,simply as in the nature of a rat psychologist's accordancewith thisprediction based on our degreeof polyg- ratiocinations offered free' [85]. Keeping in mind. then, that yny, we humansshow sex differencesin staturethat vary the differencesare small,how do men and women differ in between4 and ro per centamong cultures [3r]; in contrast, cognitiveability? the Northern elephantseal (Mirounga angustirostrls)male, Women excel in tasks requiring forms of fluency.or what whocan maintain exclusive access to a largeharem of females, might be described as a rapid deployment of attention and may weighthree times as much as an adultfemale [4]. skill. For example, the largest female advantage is seen in Hence,similar body sizein men and womenalready sug- 'motoric fluency', where fine motor skills must be used to geststhat there are only small socioecologicaldifferences place pegs into holes, or objects must be constructed by betweenthem and that sexdifferences in cognitiveor neural putting things together in a specified order. Verbal fluencv. sexdifferences might alsobe smallor insignificant.Such dif- such as the ability to list words beginning with a prescribed ferences are indeed small [zo]. They can also be elusive, Ietter, also shows a female advantage[zo]. Finallv.women varyingfrom study to study.Only too often the conclusion outperformmen on tasksrequiring'attentional fluency': the reachedby a seriesof studieson a particulartrait is that the ability to identify rapidly similaritiesor differencesbetrvecn magnitudeof the differenceis slightand sensitiveto experi- objects,match objects by their similarities.or find one svmbol mentalconditions. Perhaps fuelled both by this uncertainty amid distractors.Mathematical diff'erenccs. such as thc solu- and the universalinterest and importanceof the issue,hun- tions to algebraicequations, can also be calculatedmore dredsof researchershave studied the effectof sexon cogni- quicklyby women than by men [5r]. tive ability[S:, S+]. In recentsummaries of thiscontentious Perhapsakin to'attentionalfluency' is a woman'sabilitv to literature,few cognitivemeasures show a strongeffect size unconsciouslynotice and rememberthe locationsof otrjects. (definedas the number of standarddeviations between group and to recognize,more quickly than men. that an object has means).Yet becauseof the importanceof the question(i.e. been moved or taken away.When collegestudents are asked whether men and women differ in intellectualability), I to study a drawing of a random array of common or unfa- concur with SandraWitelson's conclusion: Although they miliar objects,women remember the locationsmore accu- havelittle, if any,practical significance for anyindividual, such rately.Women also remember the locationsof objectsin a differencesmay havemajor theoreticalsignificance, [qS]. room in which they were asked to wait briefly [26, 8o]. It is as if women are keeping a continuousrecord of the visual imagesin their environment.This is also seenwhen they are ses'differences in human cognition moving around in space;ineither tabletopor full-sizespatial mazes,where a route must be traced or walked between two Sittingin my officeinTolman Hall,I am remindedthat before points, women are more likely than men to remember the discussingdata on humans,I can do no better than to quote landmarksen route to the goal [3o,5i], similar to the female 66 67 Luciu Jttcobs SexualdifJ'erentiation und cognitiveflmctiort laboratoryrats, noticing and remembering more details about detectedby imposingan interveningdistractor task. Because theirenvironment. processingcapacity is limited. two tasks that use the sanre The femaleadvantage is, however, never large. Large cog- resourcesinterfere with each other, and henceperformance nitive sex differencesare found only in spatialtasks with a on either task declines.On average,a woman'sperformance male advantage.The mostconsistent task to showthis male declinesif shemust solve an irrelevantverbal (but not spatial) advantageis the Shepard-Metzgarmental rotation test task and the oppositeis true of men, whose performanceis whereone comparesand matchesthree-dimensional oUiects affectedonly by interveningspatial tasks Ir4]. by mentallyrotating the novelobject into the sameorienta- tion as the sample[41]. For cognitivesex differenc,:s,these are largeeffects [zo]; although, to put thesedifferences into D evelopment and differentiation perspective,sex differencesin height show effectsizes that are twice as large as thoseseen on mental rotation,which Cognitive systemsin birds and rodents are critically tied to showsthe largesteffect size in a humancognitive sex differ- the posthatchor postbirth interval:experimental manipula- ence[34]. tions of the developmentalhormonal environment demon- Justas worl3:t :3em to excelin noticingmany things and stratethat sexualdifferentiation of songlearning and spatial changingtheir attentionquickly, men seemto excelat tasks learningare due to the actionof steroidhormones. and hence with the oppositerequirement: those that require the single- are a consequenceof geneticand gonadalscx deternrinatiort. mindedpursuit of a goalthat involvesthe representationof Thus the developmentand differentiationof cos,nitivesex direction.For example,men throw projectilesmuch more differencessuggest that the underlyingnre chanisnr is sinrilar accuratelythan women, although there are no sexdifferences in thcsetwo typcsol'learnirrg. in theability to blockthe same projectile [89]. Men learn maze The similaritiesin the useof spatialstrategies bv maleand routesmore quicklyand with fewererrors than women,and female mammals (at least,in rats and humans)suggest that canreverse directions on themaze with fewererrors, although spatial ability in humans might also be organizedbv peri- theyremember fewer details about the route they have taken. natal hormones.This questionhas. been addressedwith data This also appearsto be a spatialrepresentation based on from situationswhere disease,pathology. or abnormalgeno- compassdirection, rather than route finding in relationboth type haveproduced abnormal hormonal environments in the to landmarks andcompass direction as in women[So].Again, developing human Izo]. thissex difference in cognitivestyle is remarkably reminiscent For example,in the caseof girls with congenitaladrenal of that observedin malelaboratory rats, who preferto orient hyperplasia,the adrenalglands. which normally producelorv to distant cues offering direction information rather than levelsof androgen,produce excessiveandrogens prenatallv. deducingtheir location from the arrayof visiblerandmarks at Becausearomatase enzymes in the brain can convert andro- their currentvantage point [92]. gens to oestrogens,increasing the level of either steroid Thus, similar to results from rodent studies,men and hormone can masculinizeneural substrates;it sintply depends women differ most consistentlyin spatialtasks, and do so on the type of steroid receptor expressedby the structure. becausethey solve the problemin differentways. In the task Becausethese androgens masculinize the externalgenitalia. of mentalrotation, the typeof strategyused, whether a purely thesegirls can be recognizedat birth and successfullytreated. visuospatialstrategy or by verbalcoding of the objects,ian be limiting the excessandrogen exposure to periodsbefore and 68 69 Lucia Jacobs Sexual differentiation and cognitive function just after birth. Hence,cognitive abilities that are masculin- (diethylstilbestrolor DES) to maintainpregnancy and hence izedin thesegirls must be due to the effectof excessandro- exposurewas limited to the prenatalperiod. Girls exposedto gens on neural substratesthat differentiatedur'ng this this oestrogenshowed normal spatial ability and levels of period.One consequenceof this conditionis an increasein aggression,two factors which generally show the greatest performanceon spatial tasks such as mental rotation degreeof sexualdimorphism, although they did show a more althoughthere is no affecton verbalintelligence [zo]. masculine pattern of language lateralization [zo]. Thus. In contrast,girls with Turner'ssyndrome have lower than spatial and verbal cognitive traits appear to differentiate at normaloestrogen levels due to a chromosomalabnormality different periods in development.Prenatal hormones may (XO genotype).As adults,they showcognitive deficits both thusinfluence language lateralization but abnormalhormone in verbal fluencyand in spatialvisualization [66]. Because levels must continue into postnatal life to influence the dif- they seemto be handicappedin a diversegroup of tasks,it ferentiation of spatial abilities.This may be similar to the hasbeen suggested that theirdeficit can be definedas'pro- pattern seenin rodents,where spatiallearning in femalesis cessingspeed and attention' [zo]. In other words,perhaps influenced both by pre- and postnatal oestrogen levels. they lack preciselythat attentionaland perceptualfluency whereas the male strategy of spatial learning is influenced which characterizesa woman with normaldevelopment. only by the postnatalhormonal environment[92]. Spatialdeficits can also be found in men with patho- logicallylow levelsof androgensduring development, such asin idiopathichypogonadotrophic hypogonadism. Here, the Sex differences in the braitt testesfail to be sufficientlystimulated to producenormal Ievelsof androgens.It is not clearexactly whether the andro- The evidencefor an underlyingneural basisfor cognitivesex gendeficits occur pre- or postnatally,however, males with this differencesin humansis controversialIr5. zo].Thercmust bc conditionhave significantly impaired sparial ability [37]. at leastthree reasonsfor this:first. as in cognitivetraits. only It thusappears that in humans,as in thelaboratory rodent, smallor inconsistentdifferences would be predicted.Second. it is not the geneticsex of the individualthat determines our speciesis characterizedby plasticity.with an extended spatialability, but its hormonalenvironment during develop- period of development;this, too, should affect the develop- ment.However, developmental trajectories in the brain are ment of cognitive abilities.'Ihird,the taskswhere men and profoundlyinfluenced by the relativetime period spentat women differ may call on more generalizedcognitive abili- eachdevelopmental stage [29].To understand the sexualdif- ties than those describedin songbirdsand rodents.If rve ferentiationof the brain,we mustknow bothwhich hormones cannotmap a cognitivetrait to a specializedstructure (e.9. play an activerole and when they producetheir effects.For a song nucleus)but must nrap it insteadto a constellation example,both congenitaladrenal hyperplasia and Tirrner's of multi-purpose brain structures (and even a seemingl-v syndromeresult in increasedlevels of steroid hormones specializedstructure such as the hippocampushas more before and after birth; both show predictableeffects on identifiedfunctions in humansthan the rat [52]).then. once spatialcognition. However, an excessof hormone that is again,we should not expect to find strong sex differencesin administeredbefore birth only does not appear to affect any one structure. spatialcognitive abilities. This was concluded from studiesof Thus it shouldnot come as a surprisethat men and women girlswhose mothers were treated with a syntheticoestrogen appear to differ most not in the size of a particular brain 7o '7 I Lucia Jacobs Sexual differentiation and cognitive firnction structurebut in a fundamentalfeature of brain organization: of neocortexin the vicinity of one'sears) is largerin women the degree lateralization. of The averageadult femalebrain than men It]. Another sex difference is found in the massa appearsto be more symmetricaland hence less lateralized intermedia,a tract connectingsubcortical areasin the thala- than the malebrain [6o].The consequencesof symmetryfor mus.This odd structure,present in other primate speciesbut brain function are seen in the relative robustnessof the often not found in humansat all, is more likely to be absent femalebrain in responseto stroke;beingless lateralized and in men than in women,and when present,it is smallerin men hencewith brain function redundantlyrepresented, women than in women [r]. recoverspeech more quickly after traumato the left hemi_ However, the most consistentand well-studiedsex differ- sphere[5r]. Femalebrains are lesslateralized than male encein commissuralvolume is found in the corpuscallosum. brainseven on listeningtasks, such as the accuracywith which Specifically.the differenceappears in the posteriorcallosum. the time of soundarrival is judgedin eachear (the dichotic in an area called the splenium,with female spleniahaving listeningrasx7. Men show hemisphericspecialization in this greater maximal length,greater area as a function of brain task,with a strongerright ear (i.e.left hemisphere)advantage weight, and greater total callosalarea [23].This result has than do women [39]. More recent exampleshave used been controversial;because of the importanceof this fibre brain imagingtechniques to comparethe lateralizationof tract, this result has been replicatedby many researchers: language functionin menand women. Once again, the female thoseusing exactly the samemethods as the originalstudv brain is fundamentallymore symmetrical,using both frontal havefound the sameor a smallerfemale advantage. although corticesto solve a verbal task such as rhyming;-duringthe male thoseusing other methodshave found no difference The brain uses_ [:o]. predominantlythe left hemisphere the samepattern hasalso been describedin rats:the spleniumof sametask [77]. the corpuscallosum is larger in femafesthan males[46]. A symmetricalbrain requires a greal3r coordination of effort to processsimultaneously information in both hemispheres.Hence. the pathwaysconnecting the cerebral The developnzent of lateralized .function hemispheresshould be more extensivein thi symmetrical brain. For example, both men and women who represent How do such sex differencesin laterality differentiate?If speechprimarily in the right hemispherehave a signihcantly Iaterality is associated with differences in cognitive largercorpus callosum, the main fibre tract connectinsthe ability,which are themselvesstrongly influenced by perinatal left and right cerebral hemispheres,than peoplewho rfpre_ hormones,then brain laterality may also be hormonalll, sent speechin the left hemisphereonly [7o].Thissuggests ihat mediated. bilateral representation of function,whether in males or Evidence from songbirdsand laboratory rodents suggesr females,is relatedto the size of fibre tractsconnecting the that steroid hormonesdo influencethe developmentof sex two sidesof the brain. differencesin lateralization of brain structure and function However,on average,the size of thesecommissut.es shoulc For example.the male canary'ssong production is severelv be largerin womenthan in men.There seems to be someevi_ disruptedby severingthe left, but not the right. nerve which dencefor this in three largefibre tractsthat connectleft to innervatesthe syrinx [69].Male gerbils(Rodentia: Meriones right cerebrain humans.The anterior commissure,a fibre unguiculatus)show structural asymmetry in the brain nucleus tractconnecting left andright temporalneocortices (the area involved in their ultrasoniccourtship call. rvhichis larser in 1a IJ Lucia Jacobs Sexual differentiation and cognitive fttnction the left than right hemispheres;more important, the devel- are related to a general difference in cerebral symmetry: the opment of this lateralization depends on the presence of male brain tends to be more asymmetricthan the female testosterone[+o].Finally, there are more generalizedeffects brain, which correlateswith smaller volume of interhemi' of steroidhormones on lateralizationof structureor function: sphericcommissures. Such structuraldifferences are deter- female rats exposed to postnatal androgens show a mas- mined not by geneticsex but by the postnatalhornlonal culinizedDattern of lateralizedmovements [24,92]. environment; experimental manipulations or hormonai Similaretlects may be found in humans,although the data abnormalitiesor perhapssexual orientation are associatccl must be interpreted cautiously.One example is iateralization with predictableshifts in the degree of lateralizationanct of function in women with low oestrogenlevels:Turner's syn- spatialability. drome women show even lesslateralization of function in the Why shouldperinatal hormones cause such a shift.increas- dichotic listening test than do normal women [68],suggesting ing or decreasingthe degreeof symmetryin the developing that a certain level of steroid hormone is required for norma. brain? Perhaps for two reasons:first, the brain does not lateralization to develop. Other evidence comes from mea- grow symmetrically;and second,because the brain grows sures of lateralization and cognitive function in male and asymmetricaily,the iength of the developmental period female homosexuals.Because homosexuals are similar to profoundly affectsthe degree of cer,:bral asymmetry. their opposite sex in sexual orientation, rne might expect One of the first hypotheses that development is often cognitive similarities as well, if such traits,have a common inherentlyasymmetric derrves from the observationthat the developmentalorigin. Some studieshave found that gay men left and right sides of a developing embryo responded dif- scorelower than heterosexualmen on spatialtests [74]. Gay ferentlyto experimentalmanipulations. suggesting that some men also show lesscerebral lateralization than heterosexua- cytoplasmicfactor appearsto be respcinsiblefor the fornrtt- men,since the sizeof the anteriorcommissure is largerin gay tion of an innate left and rig_htside (describedin Morgitrt than heterosexualmen [z]. In addition,homosexuals shorv [63]). In r978, Michael Corballis and Michael Morgan pro- different patterns of functional laterality on dichotic listen- poseda new theory of brain lateralizationbased on this idezr ing tasks:neithergay men nor lesbiansshow the widely repli- lzz,64).Arguingthat all growth is asymnietricaldue to innate cated pattern of perceptual asymmetry with consistent properties of the egg's cytoplasm,they proposed that this right-handedness.In other words,being right-handedpredicts asymmetry also shows an innate bias for the left side tct a strongright ear biasin heterosexualsbut not h<,mosexuals precedethe developmentof the right side.Eventuallv. the [58].All of this is consistentwith the idea thar hormones, right sideof the brain,given enough developmental time. mav development,and degree of cerebral laterality are somehow catch up with the left and produce a symmetricalstructure. inextricably linked. But should development continue further. the right mav surpassthe left and a right bias could eventuallydevelop. Hence,the longer the development,the more potential for Laterality and rates of development asymmetry exists, and the more lopsided a brain might become,as seenin our own species,the'lopsided ape'[zr]. The male and female mammal (at leastin laboratory rodents Subsequent researchershave improved on this theory; for and humans) thus appear to differ most dramatically in the example,Ursula Mittwoch has suggestedthat maturational domain of spatial cognition.These cognitive sex differences gradientsmay start with the left but then switch to the right. 74 75 Lucia Jacobs Sc.rttrtld iffa rcn Ii u t i rt t r art d cogt t i Ii vt' ftut c'Ii tttt Thus,in any structurethe directionof asymmetryshould be or XXY genotype),experience higher than nornral steroid predictablefrom its developmentalage, relative to other hormone levels,develop more slowly than the normal XY structures.Waves of developmentproceed down the body, genotypemen, and have lower verbal abilitiesrelative to headto toe,and the longer a structurehas been differenti- spatialabilities Iro]. ated,the greaterthe probabilitythat its asymmetrywill have These are the extremes, however. If the growth vector proceededfrom left-biasedto right and then back to left, hypothesisis correct,then normal sex differencesin spatial explaining,for example,why arms and legsshow different ability could be a manifestation of the grorvth rates of men patternsof lateralization[6r], and women rvhich produce differentialgrowth of the cere- Yet eventhis model may be too simple.In her'growth bral hemispheresand hence differencesin laterality'If so. vector' hypothesis,Catherine Best incorporatesnot only then an individual'srate of maturationshould predict the dif- left-rightdifferences, but alsoanterior-posterior and dorsal- ferentiation of late developing structures and hence their ventralvectors. In the humanbrain:'The overall effect on the level of spatial cognition. hemispheresis as though some force had twisted the left In tg76, Deborah Waber found that sex differences in hemisphererearward and dorsal,while twisting the right spatial ability were a consequenceof sex differencesin age hemisphereforward and ventral'.The result of theseonto- at puberty;late-maturinggirls showed superior spatial ability. geneticcontortions is a differentallotment of tissueto the Thus,the differencebetween boys and -girlscould be ascribed two hemispheres,with a concomitantchange in commissural not to sex but to age at puberty and it appearedthat cogni- volumeto accommodatethe coordinationof two,more sym- tive sex differenceswere a result not of sex but of nratura- metricaland hencemore equal hemispheres,And because tion rate,which, on average,is associatedwith sex [88].Her brain structuresdevelop in a roughphylogenetic order, with initial finding was basedon girls from extremesof the nlatu- 'primitive' areas,such as primarysensory and motor areas rationdistribution: subsequent attempts at replicatit-rnfailecl developingbefore areasthat associatethese inputs, Best when such extreme maturation groups werc Ilot uscd. hypothesizedthat such tertiary associationareas should However. a more recent summary of these studies has developlast in the right hemisphere.Therefore, an increased confirmed this effect, although the effect size is probablr' developmentalperiod should be associatedwith enhanced much smallerthan originallyreported [:6]. higherfunctions of theright hemisphere, such as visuospatial There is a suggestion that this relationship i'retrveen functionsIro]. the rate of maturation and cerebral lateralizationciin irc ln accordancewith this hypothesis,it appearsthat the found in men and rvomen of normal genotype but honro- rate of maturation may indeed predict traits associated sexual orientation.As describedearlier. homosexual Inett with symmetry:the degree of cerebral asymmetry,the appear feminized in regard to measuresof laterality and volumeof the cerebralcommissures and the level of spatial spatial function. They also reach puberty earlier than ability. Once again,there is evidencefrom humans with heterosexualmen [56],and are of smaller stature Irz]. The chromosomal abnormalities.Turner's syndrome women pattern of cognitivedevelopment in lesbiansmay be quite (XO genoLip;)show an increasedprenatal development different from homosexualmen: they shorveither similar or '; rate,an.i ll is associatedwith greatercerebral symmetry lower performanceon spatialtasks than heterosexualrvonren andpoorer spatial ability than women with a normalXX geno- [59, 86], but it is not clear how this relatesto their rate of type.Incontrast, men with supernumerary-X syndrome (XXX maturation. 76 77 Lucia Jacobs Sexual differentiation and cognitive function Thus,evidence for a relationshipbetween the rateof matu- the process of longitudinal bone growth. Most structural ration,lateralization,and cognitivefunction may be present growth is reachedby late adolescence,though approximately in at leastthree groupswho appearto differ in their early one to two years earlier in girls than boys,at least in west- hormoneexposure: individuals who vary by chromosomal ernized societies.This produces a sex difference in stature. abnormality,who differ by sex,or who differ by sexualori- since slower maturing individualswill be taller when thev entation.Hence, regardless of the proximatecause, the hor- reachthe stageof skeletalmaturation [83]. monal environmentappears to direct the developmentof What is the adaptivesignificance of such sexualbimatur- cerebrallateralization. This developmentaltrajectory then ism? It appearsto be an adaptationfor polygamyin manr producessubsequent changes in cognitiveability, most species[4], based on the followinglogic. Small males cannol noticeablyin the realmof spatialcognition, as would be pre- competefor accessto femaleswhereas small femalesare not dicted from its late developmentas a tertiary,right hemi- handicappedby their body sizesince the female'sslorv rate sphereassociation area. of reproduction assuresthat they will be the limiting sex. Hence, males will compete for females and hence males.not females,will require a larger body size to compete Ir9]. In Sexualselection and laterality highly polygynousspecies. where body size dimorphism is most pronouncedand male reproductivesuccess is strictlv Yet such correlationsbetween development and function tied to body size, delayed maturation thus functions to simplyrelocate the questionof cognitivesex differences to a increasecompetitive ability [a]. more proximatelevel of analysis;they do not addressthe Therefore,the consequencesfor the rate of maturation questionof why malesand femalesshould mature at differ- can be subject to sexual selection.Other consequencesot ent rates.To answerthis question, one mustleave the realm maturation rate, such as the differentiallateralization ot' of cognitiveneuroscience and returnto that of evolutionary the brain and hence differential cognitive ability. could biology. also be the product or side-productof sexualselection. A The most commonexplanation for sexualbimaturism is simple model could be constructedfrom the basic biologv thatit isa mechanismby whichsexual selection can act on the of cerebral growth vectors and sex difference in the rate differentialallocation to trait size.For example,climorphism of maturation that would explain sex differencesin cere- in body sizeis a commonsexual dimorphism. It is alsothe bral lateralization and spatial function. If this model is direct consequenceof differentialgrowth patternsbetween correct, then sex differencesin cognitive function would malesano lelr,ales.Because growth for many vertebrate be influencedby any factor that changesthe rate of deve-l- speciesessentially halts at puberty,individuals that mature opment. The laster the rate of gro',vthor tlre earlier thc more rapidly reach puberty at a smaller adult size.Thus, date of puberty,the more cerebral symmetry,less right henri- simplychanging development rates produces sex differences spheredevelopment, and henceless specialization of spatial in traitsize [4]. function.If pubertyis extremelyearly, one would predictthat In humans,sex differencesin statureare also correlated left hemispherefunction achieves an unnaturaldominance: if with the age at puberty.Girls developmore quickly than puberty is extremely late. then right hemispherefunction boys,reaching the developmentalstage where androgens halt should excel. 78 79 Lucia Jacobs Sexual differentiation and cognitive function Food, sex,and cognitivefunction could be a physiologicalresponse to socialstress, since girls reach puberty earlier in householdswhere the father is What factorsinfluence the rate of developmentor age at absent[8r]. However,because diet is directlylinked to thc puberty?One of the best studiedexamples is the t ffect of reproductive functions,such as hormone levels.ovulation socialcircumstances, such as social class, westernization, or an frequency,etc. in humans [28], it may play an extremell' urbanlifestyle.This is clearlyreflected in the patternsof body important role. Under more natural conditions.such as stature:over tne last century,perhaps due to a twentieth- non-industrialcultures, diet may have an even larger effect centurychange in diet,children have become progressively on human physiology.In a study of endocrineresPonses largerat all ages,resulting in an increaseof aboutone inch in New Guinea hunters, Carol Worthman reported that per generationin addedheight. As a result,both men and testosteronelevels were twicc as high in rich as in poor womenachieve a greaterstature, and attainit in feweryears men [97]. than they did a century ago.These patternsare strongly A consequenceof the human'ssensitivity to environmen- influenced,however, by socialcircumstances:poorer boys are tal conditions is that rates of maturation may vary drama- significantlyshorter than wealthyboys at all ages[83]. tically by culture. In New Guinea hunter.-gatherersocieties. Becausestature is relatedto ageat maturity,this suggests puberty is not only delayedrelative to industrialcultures. but that childrenare maturingat youngerages. Indeed, the age is also more protracted;thetypiral growth spurt seenin the at puberty in girls has changeddramatically over the last westernadolescent is seenas a much more gradualincrease century.Using the ageat first nienstruationas an unambigu- in growth rate. As a result. adolescent girls and bovs ous indicatorof maturationin girlsin six westernsocieties, show more similar rates of growth: one might predict an J.M. Tannercalculated that thisage has dropped four years absenceof sex differencesin brain organization for this in the last century,a rate of approximatelyfour monthsper reason.However, this effect is mitigated in Nerv Guinea decade,although the trendnow appearsto havestabilized at becauseof differential treatment: boys are valued more an averageage of twelveto thirteen1'ears [83]. highly by parents,and thereforeare fed higher qualitv foods. This patternalso appears in contemporarycultures which and hence this potential for developmental equality is differin theirwealth andsocial class, and thus perhaps in diet. not realized[q6l Even so.the sex differencein the ase at Daughtersof unskilledworkmen in Britain reachmenarche puberty is smaller in non-industrializedsocieties. In this two to threemonths before daughters of men with manage- sense,the protractedadolescence, rvith early sexualmaturity. rialjobs [89]..Asimilar pattern is foundbetween girls living found in western societiesmav be a recent artefact of our in urbanversus rural areas: the averageage of pubertyin girls urban culture [79]. livingin Warsawhas been almost two yearsyounger than girls If growth accelerationexaggerates the sex differencein the living in the surroundingcountryside for the past hundred age at puberty,when both males and femalesare developing years[82]. Similar patterns can be seenin comparisonsof at their maximum rate, this could theoreticallyproduce a urbanand rural populationsin Nepal,Bolivia, and the United greater difference in cerebral laterality, with a subsequent States[5]. increasein sex differenceson spatial tasks.This model would Thesedifferences are probablycaused by a multitudeof reconciliatetwo contrary observations:first, that patterns of factors,including diet, exposureto disease,stress, and even cognitive sex differences in humans are highly conserved socialenvironment For [8:]. example,the rateof maturation across cultures [:+]; and second. that there are equally 8o 8l Lucia Jacobs Sexual differentiation and cognitive fitnctiort striking effectsof social environment on the development of same age with more sedentary duties. On average, this cognition in humans. meant that boys scored higher than girls on spatial tests. Researchon social effects on cognitive development has however in the few caseswhere girls roamed farther, they concentratedon the tasks which show the largest effect size alsoshowed superior spatial ability comparedto boysof their (i.e. spatial tasks showing a male advantage).Studies of age [65]. spatial cognition in different societiesand cultures suggest Thus,sex differencesin spatial cognition may be enhanced that the magnitude of sex differences are highly dependent or reversedby the socialenvironment. They may alsobe com- on environmentalconditions and personalhistory. In short, pletely eliminated.In nomadic cultures,such as the Inuit, when individuals are given more freedom to explore their where both men and women forage for food over large areas, environment, this freedom is correlated with enhanced there are no sex differences on any measure of spatial spatialabilities, both within and betweencultures, producing cognition [9]. either a male or female advantage,depending on the spatial Is there an underlying neural basis for these cultural ecology of the sexesin that culture (reviewed by Mary Van patterns? Would, for example, greater mobility as a child Leeuwen [87]).Thus, the male advantagein spatial cognition lead to enhanced function in the brain structures mediat- is seenin traditional Mexico city households,where girls are ing spatial learning? For example, early spatial experience kept at home and boys are free to wander,whereas the iden_ could increase hippocampal development and enhance tical methods,testing a ten-year sample of schoolchildren cerebral asymmetries by increasing right hemispheric in Austin, Texas,revealed onry smail and insignificant dif- growth.Although we have no data on humans,in laboratorv ferences. In Israel, the pattern of sex difference varied mammals such as the rat, the hippocampuscontinues to with Jewish subculture:among SephardicJews, men out_ add new neurons throughout life [3. 7. -50]:this is also performed women, but the reverse pattern was seen in found in other mammals (reviewed by M.S. Kaplan [-19]). Ashkenazycommunities, The female advantageseen in the This rate of neurogenesisin the hippocampusappears to be Ashkenazy community might be explainedby the arypical related to learning,as it is linked to a physiologicalprocess social organization of this culture. In a study of orthodox underlyingassociative learning, long-term potentiation[q8]. Jewsin New York City,the Sephardicpattern was seen in less The hippocampusalso respondsto changesin the environ- traditionalhouseholds: males scored higher than femaleson ment, even in adults.Adult rats moved to complex, semi- spatialtasks.The reverse was seen in more traditionalhouse- natural environmentsshow structuralchanges in the brain holds, where women obtained the highe:r spatial scores. after only four days,including an increasein structure in the The explanation offered by the author is that in strict ortho- hippocampus [45]. Finally, male rats moved to an enriched dox families, women, not men, travel outside the home to environmentshow changesin lateralityin the hippocampus: obtain goods and servicesand hence are more mobile than at puberty, the dorsal hippocampus changesfrom a greater men, who are expected to remain in seclusion for serious thickness of the right to the left side [25]. These scattered. intellectual study [87]. and not always consistent, lines of evidence suggest that such plasticity can also be distinguishedwithin a culture: hippocampal plasticity,and perhaps spatial cognition, in the in rural Kenyan cultures, regardless of sex, children who laboratory rat can be influenced by the social and physical wander farther from home, becauseof duties such as herding environment around the time of puberty. It is perhaps not livestock,score higher on spatial tasks than children of th! so far-fetched that in humans, too. social influences have 8z d3 Lucia Jacobs Sexualdifferentiation and cognitivefirnction of the brain may also organizationaleffects on brain structure,cerebral symmetry, and not the other,so sexualbimaturism greaterplasticity' Environ- and spatial ability. be part of a larger adaptationto changeseven nlore In summary, the developmental cascade leading to the ments change;the social environment with similar skills ano sexual differentiation of spatial cognition is determined- quickly, sinCeconspecifics compete by plasticityand but only by the environment, The environment may exert uuititi"r [go]. our speciesis characterized for patterns of its influence in different ways and at different times, begin- adaptabiiity, and perhaps this is also true species. ning with tnc prenatal hormonal milieu, affected later by sexual dimorphisms in cognition, as is true in other according the perinatal influences of diet and other determinants of If sexualdimorphism in heightvaries dramatically postnatalendocrinological state, and finally influenced by to diet and culture, then perhaps cognitive sexual dimor- to cxpcri- the culturally determined potential for exploration by the phisms.snrall but persistcnt.reversiblc irccording selected child.Thus, on the one hand,sex differencesin cognitivefunc- .n.., ur. simply a subtler example of a sexually under tion in humans,like those found in rodents and songbirds, predilection for a male advantageon certain tasks may be the end-product of a long developmental cascade, averagecircumstances. canalized by the early hormonal milieu, which is in part Why would suchan advantageexist in Honto sapiens?Cog' determined by genetic mechanisms.On the other hand, if nitive sexdifferences in songbirdsand rodentsoperate in the competition. and have suchdifferences are determinedby sucha ;eneral trait as an context of mate choice and mate individual'srate of developmentthen ther;edifferences are evolved in response to sa'iual sel':ction for competitive extremely plastic. Thus, if rate is key, then sex differences ability. Are sex differencesin human spatial abilities also are not'determined'at all-or only in the most minimal sense subjectto sexualselection? I can only join others in specu- of the word. lating on the possibleadaptive significance of our snlall scx differencesand their effecton the courseof human evoluticltt hunter [8o].Thescenario can be describedas follows: man the Sexual selection and human ecology requiresskills in throwing,aiming, and navigationin order to navigate long-distancehunting trips over large or unknorvn Yet even in the midst of this complex array of environmen- terrain,kill gamewith projectilesand then return home,often tal influences we can discern faint echoes of the sexually with a heavymeat burden, via the shortestroute. Thus' hunter selectedpattern seenin other species.Even the rliversityof skills tap into the same spatial abilitiesassessed by labora- theseinfluences cannot conceal the observationtl rat in most tory tasks,which would explainthe common male advantage cultures,when there is a sex difference in spatial cognition,it on suchtasks. Such navigationalskills would be adaptivefor more often shows a male, not a female, advantage.What is long-rangehunting, but not necessarilyfor short-rangegath- the significanceof this pattern? Again, the answermust lie in ering.Here, the ability to remember the location of fruiting the evolutionary history of sex differences;the magnitude of plants,notice and remembersubtle changesin spatialdistri- a sex difference may be explained by an individual's history bution of food sources,and possessfine motor control for but the average direction of the difference can only be harvestingand processingfruits and seeds,rvould be advan- skills explainedby the history of the species[38]. tageous.Thus, the female constellationof cognitive Just as sexual selection may produce sexual bimaturism would adapt for gathering,which requirestracking the fine- becauseof the advantageof increasedbody size to one sex scale spatial distribution of fruiting plants, and also have 84 85 Lucia Jacobs Sexualdifferentiation and cognitivefimction the fine motor control to manipulateand cleansmall food larger, more flamboyant coloured, more aggressive.more items. robil", more active in courtship,and more likely to bear One could thrrs interpret sex differencesin cognitive structuressuch as antlers,manes, and large canine teeth that skills as indicationsof selectionfor competitiveability in are of little or no usein exploitingnutritional resources' [35]' foragingbehaviours such as huntingand gatheringwomen, Thus,it is female,not male body sizethat is optimizedfor the not competingfor mates.This hypothesis, suggested and elab- species'secological niche; the larger size of the polygynous orated by Irwin Silverman and Marian Eals, seemingly male servedonly to increasehis ability to competervith other reducesthe needfor sexualselection to act on the evolution males,and hencewas adaptivebut not'ecological" of such sex-specificabilities, since natural selectionfor Similarly,a Martian visiting our plaiet for the first time foragingskills would be sufficientto explair the differences might note that one-halfof the populationuses their entire [8o].Yet we can neverreally know to what extentevolution- brain to processinformation, automatically integrates more ary processessuch as natural and sexual selection can explain incidentalinformation, is lessaggressive and more coopera- sexdifferences in spatialability in our species.Sexual selec- tive,and overall seemscloser to the ideal designfor a naked tion could still play a role: even in this Thrzanthe Hunter, ape.This Martian might view traits such as superiormathe- Janethe Gathererscenario, hunting prowess may affectthe maticalability or superiorskill in chessas arbitrary skills that outcome of mate competition.In fact, good hunters are have evolvedfor the samereason as a peacock'stail, repre- more attractiveto women,even if what they hunt is not a sentingthe'investment' needed to competesuccessfullV rvith necessaryor efficient addition to the group's energetic other males (i.e, the typical solution of the disadvantaged requirements[r3]. In the Ache cultureof easternparaguay, sex).It is usuallythe male'ssolution: the ability to compete wheremen must rangewidely in searchof meat and honey, with other malesusing traits that serveno otherpurpose but the families of good hunters do produce more ;urviving to compete.This view of things puts a new slant on the olcl offspring,suggesting that women should choosemates by problem of genderand society.Suddenly' the smallerfentale their huntingability [a8]. brain is seenas a miracleof economyand design'destined to survive the turmoils of history,less likely to be disturbed during development or to suffer immune disorders [84]' less Thepeacock's brain likely to becomeinvolved in unnecessaryand damagingacts of aggressionand warfare.Thus, it is the female that is thc 'ecological' PerhapsMontaigne was right and men and women,save for smaller,the sex,best adaptedto survivein thc cultureand education, do not differ that much.perhaps even ecologicalniche of the species,and it is the male rvho carries with 85 per centof our societiespolygynous, we will nlver be the heavierburden or handicap[qq] of sexuaiselection' hrs a stronglypolygynous species, and hence differences between fitnessdependent on arbitrary traits that reduce his com- the sexeswill alwaysbe subtle.Is this the end of the story?I petitive ability as a human being,although they are all to 92 93 Lucia Jacobs Sexual differentiation and cogrtitive furtctiort 'sexual 76. 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