Lateralised behaviour in first trimester human foetuses

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Pergamon

PII] S9917Ð2821"86#99045Ð4

Neuropsycholo`ia\ Vol[ 25\ No[ 5\ pp[ 420Ð423\ 0887 Þ 0887 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:87 ,08[99¦9[99

Lateralised behaviour in _rst trimester human foetuses PETER G[ HEPPER\ GLENDA R[ McCARTNEY and E[ ALYSON SHANNON Fetal Behaviour Research Centre\ School of Psychology\ The Queen|s University of Belfast\ Belfast BT6 0NN\ N[ Ireland\ U[K[ "Received 19 Au`ust 0886^ accepted 18 Au`ust 0886#

Abstract*Behavioural lateralisation is a common feature of everyday behaviour\ most familiar in the exhibition of handedness[ Despite di}ering theories about the origins of laterality\ little is known about their ontogenesis[ This study observed the left and right arm movements of 61 foetuses at 09 weeks of gestational age\ the _rst age at which lateralised behaviour may be observed[ There was a highly signi_cant preference for foetuses to move their right arm more than their left arm\ 74) exhibiting more right arm than left arm movements[ There was no di}erence in the amount of movements exhibited with the preferred arm\ whether it be right or left[ Laterality of behaviour at such an early gestational age "probably as early as it is possible for it to be observed# is unlikely to be under brain control but is probably of more muscular or spinal determination[ The possibility that early di}erential motor behaviour may contribute to subsequent laterality of behaviour and asymmetrical brain growth\ must be considered[ Þ 0887 Elsevier Science Ltd[ All rights reserved Key Words] handedness^ foetal movement^ brain asymmetry^ behavioural development^ foetus[

made in elucidating the proximate mechanism underlying lateralised behaviour and:or brain asymmetry[ Recently\ interest has turned to tracing the devel! opmental origins of lateralised behaviour in the human[ Two studies have observed lateralised behaviour in the human foetus[ Observation of foetuses using ultrasound from 04 weeks of gestation to term to record foetal thumb sucking\ revealed that the foetus exhibits a preference for sucking its right thumb ð05Ł[ Furthermore this preference was observed from 04 weeks of gestation ð05Ł[ In another study\ ultrasound was used to observe the position of the foetus|s head relative to its body in utero from 01 weeks of gestation to term ð06Ł[ At 27 weeks of gestation\ but not before where the head was held in the mid!line\ the foetus showed a preference for having its head turned to the right relative to its body ð06Ł[ The use of ultrasound enables detailed and non!invasive observation of the behaviour of the foetus from its earliest movements dur! ing pregnancy ð07Ł[ The embryo begins to move at about 6 weeks of gestational age ð08Ł^ however these earliest movements involve the whole body ð08Ł[ At 8Ð09 weeks of gestational age\ the foetus begins to exhibit single arm movements ð08Ł\ involving just the right or left arm\ which provide possibly the _rst behaviour of the individual that could exhibit laterality[ Given that handedness is perhaps the most familiar and prevalent example of lateralised behaviour\ observations of foetal arm movements at\ or

Introduction The observation of lateralised behaviour has been of considerable interest throughout history ð0\ 1Ł[ Although considered to be present at a population level only in humans\ recent observations of humpback whales ð2Ł and primates ð3\ 4Ł suggest that lateralised behaviour at the population level is not unique to humans[ Perhaps the most well!known example of lateralised behaviour is that of handedness[ Approximately 89) of the human popu! lation show a preference for their right hand whereas the remainder show a preference for their left hand ð5Ł[ Laterality of behaviour is of interest because of its link with anatomical asymmetries in the brain ð6\ 7Ł[ However\ the relationship between the development of brain asym! metries and behavioural lateralisation is poorly under! stood ð6Ł[ A number of di}erent theories have been proposed to explain this presence of lateralised behaviour and:or brain asymmetry ð7Ð04Ł\ although little advance has been

 Address for correspondence] Fetal Behaviour Research Centre\ School of Psychology\ The Queen|s University of Belfast\ Belfast BT6 0NN\ N[ Ireland\ U[K[ Tel] 90121!163129 "secretary 90121 224335#^ fax] 90121 553033^ e!mail] p[hepperÝqub[ac[uk[

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P[ G[ Hepper et al[:Lateralised behaviour in _rst trimester human foetuses

near\ their _rst appearance\ may shed some light on the development of lateralised behaviour"s#[ Hence\ this paper examined the frequency of left and right arm move! ments at\ or soon after\ their _rst appearance\ to deter! mine whether there was any di}erence in their occurrence[

picture quality such that it was di.cult to clearly visualise the foetus[ At this gestational age the foetus is {free! ~oating| within the uterus and hence its body position does not in~uence its movements[ However\ there was no di}erence between the position in utero of the 61 foetus included in the study and those 04 which were not included[

0[ Method 0[0[ Subjects

1[ Results

Eighty!seven foetuses\ who formed part of a much larger study examining behavioural ontogenesis were observed[ All individuals were born at 39 "20# weeks after an uncomplicated pregnancy\ had Apgar scores of greater than 6 at 0 and 4 min\ and no perinatal com! plications[ Foetuses were all from singleton pregnancies[ Ethical approval for the study was granted by the Research Medical Ethics Committee of Queen|s Univer! sity[

The number of individual arm movements\ left and right\ was calculated for each foetus[ If the foetus exhi! bited more right arm movements than left arm move! ments\ it was classi_ed as exhibiting a preference for the right arm^ if the foetus exhibited more left arm move! ments than right arm movements\ it was classi_ed as exhibiting a preference for the left arm[ If the foetus exhibited an equal number of left and right arm move! ments\ it was classi_ed as exhibiting no preference "see Table 0#[ Of the 61 foetuses\ 43 "64)# exhibited a greater number of right arm movements\ 8 "01[4)# a greater number of left arm movements and 8 "01[4)# an equal number of left and right arm movements[ Considering only those who exhibited a preference\ 43 "74[6)# exhibited more right arm movements and 8 "03[2)# more left arm move! ments[ Two!tailed "1!t# Binomial tests "where n  total number of individuals\ x  the number of individuals in the least frequent group\ P  probability# were perfor! med[ Using all foetuses "conservatively classifying equals as left# or using only those foetuses who showed a pref! erence "n  52# the binomial tests revealed that a sig! ni_cantly greater number of foetuses moved their right arm more "n  61^ x  07^ P ³ 9[990^ 1!t^ n  52^ x  8^ P ³ 9[990^ 1!t\ respectively#[ A paired t!test comparing the number of left and right arm movements for all individuals\ revealed a highly sig! ni_cant di}erence between the number of right and left arm movements exhibited by individuals "tð60Ł  4[806\ P ³ 9[9990#[ Individuals showed more right arm move! ments "mean 3[54 ð29[10 S[E[Ł# compared to left arm movements "mean ð2[9729[06 S[E[Ł#[ To ensure there was no di}erence in the overall num! ber "left¦right# of isolated arm movements exhibited by the three groups "i[e[ those exhibiting more right arm movements\ those exhibiting more left arm movements or those exhibiting an equal number of left and right arm movements# a one!way ANOVA for total number of isolated arm movements exhibited by each group\ was undertaken[ This revealed there was no di}erence between the number of arm movements exhibited by the foetuses in each group "Fð1\ 58Ł  0[934\ n[s[^ see Table 0#[ Similarly\ comparing the number of movements exhibited by the preferred arm "i[e[ the number of right arm move! ments for those showing more right arm movements and number of left arm movements for those showing more left arm movements#\ revealed no di}erence in the occur!

0[1[ Procedure Foetuses were observed using ultrasound at 09 weeks "21 days# of gestational age[ Mothers lay in a semi! recumbent position on a standard couch and all obser! vations were conducted between 09[99h and noon[ Prior to the start of the behavioural observation\ all foetuses were scanned\ to observe the foetal heart beat and to measure their crown!rump length[ All 76 were appro! priately grown for gestational age and exhibited a heart beat within the normal range ð19Ł[ The foetus was scanned for 29 min using either an ATL Ultramark 3plus scan machine with a 4 MHz curvilinear scanhead or Dornier AI2199 scan machine with 4 MHz curvilinear scanhead[ Throughout this time\ the scanhead was moved\ to maintain a view of the foetus in which both arms\ and their movements\ could be observed[ All observations were videotaped for later independent veri! _cation of analysis[ The number of isolated arm movements of left and right arms were recorded[ An isolated arm movement was de_ned as a movement in one arm only\ without movements in other parts of the body "after 13#[ The designation of left and right arm was determined by relat! ing the motion of the scanhead on the mother|s abdomen to the changes in picture of the foetus observed on the screen[ This method enabled the determination of the front and back of the foetus and its left and right[ Three observers were used to con_rm the classi_cation of left and right arms[ Of the 76 foetuses\ agreement among three observers on the classi_cation of arms as left or right was reached in 61 cases and thus the analysis was performed on these 61 foetuses[ Of the 04 foetuses in which agreement was not reached\ nine were moving so actively in utero that it was di.cult to follow the foetus[ The remaining six were of poor

P[ G[ Hepper et al[:Lateralised behaviour in _rst trimester human foetuses

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Table 0[ The mean "and standard error# number of isolated arm movements for foetuses who showed more right arm movements "Right#\ more left arm movements "Left#\ and an equal number of right and left arm movements "None#[ Number of Isolated Arm Movements Total "L¦R#

Right

Left

Arm Preference

n

Mean

S[E[

Mean

S[E[

Mean

S[E[

Right Left None

43 8 8

6[86 6[56 5[56

9[20 9[72 9[56

4[19 1[56 2[22

9[10 9[36 9[22

1[66 4[99 2[22

9[05 9[51 9[22

rence of preferred arm movements "tð50Ł  9[247\ n[s[^ see Table 0#[

2[ Discussion At 09 weeks of gestation\ human foetuses exhibit lat! eralised behaviour\ moving their right arms more than their left arm[ Although the proportion of foetuses exhi! biting more right arm movements is slightly less than the population level for right handedness "76[4) vs 89)#\ this is well within the range found for right handedness[ The _ndings support a growing series of observations of the presence of behavioural lateralisation in the prenatal period ð05\ 06Ł[ The observation of lateralised behaviour so early in gestation\ has implications for the developmental origins of such behaviour[ The exhibition of behaviour before birth here rules out the in~uence of postnatal factors[ More likely\ genetic factors are responsible in some way for their occurrence[ Despite di}ering theories to explain the appearance of handedness\ it is conventionally believed that hemi! spheric brain lateralisation or brain asymmetries lead to later handedness and behavioural lateralisation ð10Ł[ Researchers have sought to explain the development of brain asymmetry as ultimately arising from genetic pre! programming ð10Ł with a variety of proximate mech! anisms postulated to explain the anatomical asymmetries\ e[g[ di}erential hemispheric cell growth or cell elim! ination ð10Ł[ The observation of behavioural asymmetries during the _rst trimester poses some intriguing and di.cult ques! tions for this view of the development of behavioural lateralisation and the development of other lateralised behaviours and asymmetrical brain structure[ At present\ the earliest anatomical evidence of brain asymmetry\ that present in the Sylvian _ssure at 05 weeks ð11Ł or Heschl|s sulcus at 20 weeks ð12Ł\ is some weeks after the _rst exhibition of behavioural lateralisation[ At this stage of development\ motor function is considered under mus! cular or spinal control rather than that of the brain ð07\

13Ł[ Hence\ it is di.cult to see how the brain could be responsible for the di}erential motor activity[ Although the relationship between behavioural lat! eralisation and CNS asymmetry is not clear ð6Ł\ the obser! vation of behavioural lateralisation prior to structural asymmetry suggests it may contribute to subsequent CNS asymmetry\ i[e[\ di}erential motor behaviour precedes and determines neural development[ It is well established that stimulation may in~uence brain organisation ð14\ 15Ł and it may be that prenatal behavioural lateralisation results in the development of brain asymmetry[ Asym! metric motor behaviour may di}erentially stimulate the brain and result in di}erential development of left and right hemispheres[ The initial cause of di}erential motor behaviour is unknown but genetic factors may well pre! dispose advanced right!sided motor development[ Whatever the causal link and subsequent development of behavioural laterality and asymmetric brain function\ lateralised behaviour is present possibly from as early as it is possible to observe such behaviour[ This suggests that from our earliest embryonic origins\ lateralised behaviour is a prominent feature and a potentially power! ful in~uence on subsequent behavioural and structural development[ Acknowled`ements*We thank Prof[ K[ Brown "Psychology#\ Prof[ W[ Thompson "Obstetrics + Gynaecology# QUB\ Dr J[ Dornan "Director Royal Maternity Hospital#\ for facilities for this research^ Dr L[ Leader\ University of New South Wales\ for discussion and comments on the ms^ and the Consultants and patients of Royal Maternity Hospital\ Belfast\ for their help and co!operation[ The paper was completed whilst PGH was on sabbatical leave at Department of Obstetrics + Gynae! cology\ University of New South Wales\ and thanks are due to Prof[ M[ J[ Bennett for providing facilities whilst there[ The research was conducted with the support of grants from The Wellcome Trust\ the Medical Research Council and The Lev! erhulme Trust[

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