orientation responses to biological odours in the human newborn. initial pattern and postnatal...

8/17/2019 Orientation responses to biological odours in the human newborn. Initial pattern and postnatal plasticity by Luc Ma…

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0 Academic des sciences / Elsevier, Paris

Neurosciences / Neurosciences

Orientation responses to biological odours

in the human newborn. Initial pattern

and postnatal plasticity

Les r6ponses d’orientation aux odeurs biologiques

chez le nouveau-n6 hurnain. itat initial et plasticit postnatale

’ Laboratoire depsychopbysique sensorielle, CNRS EP 618, universitP Lou& Pasteh, IO. rue Goethe,

67000

Strasbourg,

France

2 Laboratoire de comportement animal, CNRS URA 1291 et station dephysiologie de la reproduction, Inra, 37380 Not&l& France

3 Dkpartement de psycbologie, universiti de Reims, et laboratoire de psychobiologie du developpement, &ole pratique des bautes Jtudes,

41, rue Gay-Lussac, 75006

Paris,

France

Les rtponses initiales d’orientation et leur developpement precoce sont analysees chez des

nouveau-nts exposes simultanCment a I’odeur de leur liquide amniotique (AF) et a l’odeur des

secretions lactees (L) maternelles. L’orientation relative entre ces deux odeurs est etudiee en fonc-

tion de l’hge postnatal

(1-5

j) et de l’experience de t&tee

(O-32

tetees). Avant le troisieme jour, les

nouveau-n& :ne differencient pas AF de L. Cette reponse indifferenciee est interpretee en termes

d’equivalence sensorielle et/au hedonique d’AF et de L. Apres 3 j et de 7 a 12 t&tees, une preference

en faveur de L est exprimee, refletant a la fois l’exposition repetee a l’odeur L et un changement

qual itatif du lait maternel lors de l’installation de la lactogenese. Cette sequence dkeloppementale

rhele que : i) les reponses du nouveau-m? humain au colostrum pourraient etre influencees par

l’exposition a des qualitts chimiosensorielles similaires in utero, et ii) que ces reponses sont ajustees

au changement progressif des proprietts chimiosensorielles du lait lors de la lactogenese.

Mats cl& : nouveau-n& humuin. fcefus, olfaction, liquide amniotique, colosfrum. lait maternel,

plasticit comportementale, naissan ce. adaptation neonatale

ABSTRACT

The initialpa.ttern and development of odourpreference was studied in infants simultaneously exposed

to amnioticfltrid (AF) and maternal lactealsecretion (L). Fivegroups of varying age (range: I-5 day)

and breast-feeding experience (range: S3.2 fee&)

were studied. Before postnatal c&y 3, no evidence of

differentiation ofAF and L was apparent. AjZer 3 days and 7-12 breast-feeding episodes , a rignQ ant

preference for L arised. The initial stage (days 1-3) may reflect fetal acq uisition of AF odour and

sensory/motivational equivalence of AF and L odours. The second stage (days 4-5) may reflect the

infants’perctption of change in milk quality and increasing experience with milk. Thi s sequential

development attests to a high plasticity in the initial stage of human o/facto y development.

Key words: human newborn, human fetus, olfaction, amniotic fluid, colostrum, breast milk,

behavioural plasticity, birth, neonatal adaptation

Note

prbentte par Pierre Ruser

Note remise le 15 septembre 1997, accept& aprks r&i&n le 17 novembre 1997

*Correspondence and reprints

C. R. Acad. Sci. Paris, Sciences de la vie / Life Scien ces

1997. 320.999-1005


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L. Marlier et al.

VERSIONABR&EII?

Chez pluskurs esptces de mammiferes placentaires, la s&c-

tivi tk des rkponses nkonatales envers Ies stimulations olfacti-

ves apparair dkpendante de l’exptrience olfactive fcetale.

L’information olfactive acquise in utero conscitue ainsi une

solution de continuitk sensorielle lors de la transition natale.

Une telle continuitC olfac tive transnatale a kte sugg&e dans

le cas de l’espkce humaine. Des enfants ?I& de 2 j, nourris au

sein, n’expriment pas de reponse d’orientation dphalique

diffkrentielle dans un test de double-choix olfactif prtsentant

simultan&ment l’odeur de leur liquide amniotique et l’odeur

du colostrum maternel. Cette reponse indiffkrencide a &T

interprkke en termes

de

similaritk chimiosensorielle et/au

motivationnelle des deux fluides pCrinatals ; cette similarit&

rtsulterait du transfert simultane des ar6mes de I’alimenta-

tion maternelle dans les compartiments fceta l et mammaire.

Cette etude ;apour but d’examiner deux prtdictions qui d&i-

vent de l’hypothkse de continuitk chimiosensorielie transna-

tale :

i) Le de@ (de similarice chimiosensorielle des deux fluides

devrait Ctre maximal peu aprks la naissance, lorsqu’ils sont

soumis g l’influence simultanee du profil aromatique de la

dikte maternelle. Cette similarit plus marquke entre les

odeurs amniotique et colostrale devrait alors rksulter en

l’absence de prefkrence relative chez des nouveau-n& ayant

une expkrience nulle ou trts limit&e de la t&e.

ii) Le traitement olfactif initialement indiffbrencik des deux

fluides pkrinatals devrait cependant &re rapidement mod&C

en fonction de l’%ge et de l’expkrience de t&e au sein ; en

particulier , la direction des reponses devrait Ctre mod&&e B la

fin de Ia phase colostra le, lorsque la qualiti aromatique des

s&r&ions la&es est radicalement modifiee du fait de l’ins-

tallation des mkanismes galactopokkiques.

Ces deux hypothkses sont examinkes dans une Crude trans-

versale de nouveau-n& Sg& de 5 h B 5 j et dont l’exposition au

lait varie de 0 & 32 t&es.

Cinq groupes de nouveau-n& n&s B terme (n total = 66),

equilibrks selon le sexe, sont exposts aux tests de double-

choix olfactif . Leurs caractkristiques d’%ge et d’expbrience ali-

mentaire sont prksentkes dans

le tableau I. Ces sujets

ont et6

exposCs d des tests de 2 min opposant des tampons de gaze

imprdgnks soit de 20 gouttes de leur liquide amniotique

(AF), soit d’une quantitC tquivalente des sCcr&ions 1actCes

maternelles (L). Ces stimulations sont prksenttes de part et

d’autre du visage de l’enfant, disposkes de faGon symktrique

avec une excentricite de 20-70”, et B une distance de l-2 cm

prkvenant tout contact. Mn de pallier les eff ets potentiels

d’une 1atCralisation motrice ou sensorielle, chaque sujet est

tgalement expose aux deux stimulations g droite et a gauche.

Les tests sont video-enregistrks et l’analyse des rkponses est

r&Me par un dkcodeur aveugle quant au c&C de prksenta-

tion des stimulations. Les dukes d’orientation vers l’un et

i’autre stimulus sont mesukes a l’aide du logiciel Observer.

Le crittre d’orientation vers un stimulus est atteint lorsqu’un

sujer positionne son nez au-dessus du stimulus, ce qui n&es-

site une dCviation minimale de

20”

par rapport au plan sagit-

tal. La duree d’orientation vers un stimulus est donnee

comme la proportion moyenne du temps d’orientation vers

ce stimulus en fonction du temps total d’orientation

(120 s.).

Le d&ours temporel des rkponses d’orientation relative dans

les tests de choix est present& dam la pre 1. Une analyse de

variance a deux facteurs (nature de I’odeur et groupe d’Sge/

experience de t&t&e) rkvkle des eff ets principaux de l’odeur

@ < 0,000 1) et du groupe (p < O,OOl), et une interaction

signifkative entre l’odeur et le groupe (p < 0,001). Des com-

paraisons intragroupes indiquent que les durkes d’orientation

relative entre AF et L ne different pas dans les groupes 1 ?I 3

(tableau Z). Les groupes 4 et 5 s’orientent plus longuement

vers l’odeur L que vers l’odeur AF (tableau I). Les nouveau-

n& manifestent une prkfkrence moyenne B l’kgard de l’odeur

de L aprks 72 h de vie et 7-12 episodes de tCtCes. Des com-

paraisons intergroupes r&&lent une dtcroissance de la durke

d’orientation vers l’odeur AF et, surtout, un accroissement

rkgulier de la duke d’orientation vers l’odeur L. Cet accrois-

sement vers I’odeur L est signifkati fentre les groupes 1 et 2 et

les groupes 4 et 5.

Cette etude met en hidence’un d&ours temporel biphasique

de l’orientation relative des nouveau-n& vers deux substrats

odorants auxquels ils ont ttt exposks avant ou aprb la nais-

sance. Au tours des jours postnatals 1 B 3, les enfants n’expri-

ment aucune diffkrenciation sensorielle ou hCdonique

significative des deux stimularions. Cependant, en fonction

de 1’Sge et de l’expkrience de tCtke, les enfants manifestent

une attract ion plus grande vers l’odeur L que vers l’odeur AF,

et cette diffkrenciation intervient de faGon significative aprks

le troisieme jour. Les rtponses progressivement divergentes

vers chacune des deux odeurs peuvent &re expliqu&es par

l’action de deux processus synergiques. La premike phase

(jours 1-3 et O-12 tCt&.s) semble refker,

d’une

part, une

rPponse prefdrentielle du nouveau-& ?I l’egard d’une infor-

mation acquise B l’ktat fceta l, l’odeur du liquide amniotique,

et d’autre part, un traitement sensoriel et/au motivationnel

gquivalent des odeurs amniotique et colostrale. La seconde

phase (jours 4-5 et plus de 12 t&&es) semble Stre associCe B la

perception nkonatale d’une modification qualitative de

l’odeur du lait ; aprks l’installation de la lactat ion, l’odeur des

s&r&ions lacttes dhierait de faGon croissante de celle du

colostrum, rendant la discriminat ion plus aisle entre les

odeurs AF et L. Cette skquence de rtponses pref&entielles

sugg&re que les phases Ies plus prkcoces du dCveloppement

olfactif postnatal sont g la fois dependantes des acquisitions

anttnatales et de l’exprkience nionatale. Les rCponses du nou-

veau-nt humain au colostrum pourraient Ctre influendes par

l’exposition g des qualit& chimiosensorielles similaires in

utero, et elles s’ajustent au changement progressif des pro-

pritt&s chimiosensorielles du lait qui interviennent avec la

lactogenkse.

1000

C. R. Acad. Sci. Paris, Scien ces de la vie / Life Scienc es

1997. 320.999-1005


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Introduction

The succ essful transition from the amniotic to the postam-

niotic niche requires numerous adaptations in newborn

mammals. Beside s the well-documented cardio-vascular,

respiratory and gastro-intestinal adaptations, they are

endowed with behavioural and cognitive capab ilities that

optimize early developmental adjustments [l]. Within

hours after birth, they learn how to find and seize a nip-

ple, and to obtain milk. The ir performance in these

obviously vital tasks is rapidly improved and attuned

through the experience gained from their earlier realiza-

tion. Thus , learning and underlying neural plasticity are

essentia l components of the adaptation to the postnatal

niche. However, the integrative activity of the brain is not

initiated sharply at birth [2]. The fetal brain has already

been exposed to sensory imprints and coordinated beha-

vioural training [3]. The experience-based plasticity for-

med in utero has been shown to serve the succ ess of the

very first suc:king episodes in the rat [3-51. Thus , odour

information gained in the amniotic ‘atmosphere’ constitu-

tes a tie of familiarity bridging the fetal and the neonatal

niches in this specie s. The relationship of fetal learning to

neonatal adaptation and learning has been investigated in

other specie s, including mice [6], rabbits [7] sheep 181,

and humans [9-l I].

Human evidence of perinata] olfactory continuity was

suggested in a recent report on the undiscriminative

response of 2-day-old breast-fed newborns simultane-

ously presented with the odours of their own amniotic

fluid (AF) and of their mothers’ colostrum [9]. This undif-

ferentiated olfactory response has been hypothesized to

reflect similarity of both perinatal substrates due to the

simultaneous transfer of the aromas ingested by the

mother into the fetal and mammary compartments

112, 131.

If this chemosensory continuity hypothesis is correct, it

forecasts two expectations. First, the degree of chemo-

sensory similarity of AF and colostrum (also named ‘pre-

partum mammary secretion’ [141) should be highest

around birth when both fluids are submitted to the con-

temporaneous priming of the mothers’ dietary aromas.

This greater AF/colostrum odour similarity should result in

an absence of relative preference in choice tests con-

Plasticity of odour responses in the human newborn

ducted with newborns having no or very limited sucking

experience. The responsiveness of such very young, feed-

ing-naive infants, should settle the primal stage of relative

sensory/hedonic responsiveness to the odours of the fluid

they experienced just before birth and of the fluid they

will encounter when sucking at the breast. The primal

character of this response could not be ascertained in the

sample of infants tested previously at 2 days of age [9],

because their response may have been contaminated by

postnatal exposure to AF-like cues potentially carried in

colostrum. Second, the initially similar treatment of both

fluids is expected to change with both age and feeding

experience, in the same time that colostrum is progres-

sively transformed into milk with the advent of lactogen-

esis. These two hypotheses were examined in a

developmental, cross-sec tional study involving breast-fed

newborns aged from 5 h to 5 days and whose amount of

exposure to milk ranged from 0 to 32 breast feeds.

Subjects and methods

Subjects

Sixty-six healthy term-born newborns were studied. These

infants were exclusively breast fed from birth. They were

divided into five groups according to their postnatal inges-

tive experience and age at the moment of the choice tests.

The number of subjects , age and feeding experience cha-

racteristics of each group are given in

table

1. In group 1,

six infants had no feeding experience at all at the moment

of the tests, and the remaining subjec ts had only lim ited

sucking experience in the delivery room. Mothers provi-

ded informed written consent to let their infants partici-

pate in the tests. Each subjec t was tested only on ce.

Stimuli

Two types of stimulation s were used. AF samples devoid

of blood or meconium staining were collected at delivery

and immediately frozen (-20 “C). The collection of lacteal

secretions was carried out by manual expression of

20 drops that were directly soaked (without contact with

the nipple) on a gauze pad within the 5 min preceding the

test. Both types of stimulations were presented at room

Table 1. The characteristics (number, age, feeding experience) of the five groups o f newborns studied and their relative head-orientation dura-

tions [means (M) and standart deviations (s.d.)l when exposed concurrently to the odours of their familiar amniotic fluid and their mother’s

lacteal secretions.

Relative orientation duration (s)

Groups

N subjects

Age (hi

Feeding-experience

range (N feeds)

Amniotic Fluid Lacteal Fluid

t*

P

-

1 9

2 20

3 12

4 16

5 9

M s.d. range M s.d. M s.d

9.67 4.12 515 o-1 0.368 0.205 0.239 0.127 1.62 NS

33.6 8.16 22118 2-6 0.382 0.171 0.330 0.187 0.68 NS

55.42 8.48 49-72 7-l 2 0.325 0.141 0.388 0.115 0.99 NS

85.06 7.91 7>95 13-19 0.221 0.148 0.43 1 0.136 3.3 0.004

114.22 11.79 96-l 40 >20 0.193 0.137 0.537 0.108 4.6 0.002

C. R. Acad. Sci. Paris, Sciences de la vie / Life Sciences

1997. 320,999.1005


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L. Morlier et CII

temperature on 10 x 10 cm gauze pads (100 cotton,

Hartmann, ‘Chstenois, France). T he equal amount of each

substrate used in the paired odour tests was fixed after

prior ratings of the intensity of their odour by an adult

panel [9].

Apparatus

When arousal state 3-4 [I51 was obtained, the infants

were installed in a semi-reclining seat which back was set

at a 25” angle with the vertical. Both stimu lus pads were

fastened on an U-shaped device that allowed us to pre-

sent them symmetrically on each side of the infants’ face

with an exclentricity of 20-70” (for more details about the

device, see [lo]). This device was then positioned so that

both stimulus pads were equidistant at l-2 cm from the

possib le trajectory of the infants’ nose. The infants’ visual

scene was homogenized by spreading a sheet all around

the seat; in this way the only sensory contrast they were

exposed to was generated by the olfactory stimuli and the

infants’ unavoidable head and arm movements.

Procedure

After the stiimu li were positioned symmetrically on each

side of the infants’ head, the experimenter (who stood

behind the infant) man ually turned the infants head in

order to alternately orient their nose to each stimulus pad

for 5 s. The ‘direction of this pretest orientation was syste-

matically counterbalanced for the nature and lateral posi-

tion of the first stimulus presented. The infants’ head was

then returned to the sagittal position and released after

dissipatio n of tonic neck asymmetry. Head orientation

responses were videorecorded during a first I-min trial.

The lateral position of the two stimuli was then reversed

so that the stimulus presented from the right side was pre-

sented from the left side, and vice versa. T he infants’ head

was then again oriented manually to both stimuli before

being released in the midline, and videotaped during a

second 1-min trial. The lateral position of the odour sti-

muli was controlled so that both stimuli were presented

equally often from the right or from the left side both

within and between subjects .

The videorecorded tests were analysed by a coder who

was unaware of the presentation side of the stimuli. The

head orientation durations to either stimulus were coded

by tracking the infants’ nose tip. The possib le trajectory of

180” that the newborns’ nose could scan was divided into

three an gular sectors on each side of the infants’ head: a

sector corresponding with the stimulus (labelled ‘stimulu s

sector’, ss), and two sectors corresponding with the zones

free of stimulus (covering the o-20” and 70-90” angles

with the infants’ sagittal plane; labelled ‘stimulus-free sec-

tors’, sfs). To be considered positively oriented toward a

stimulus, a subject had to position his nose over one of the

ss, which required a minimal head turn of 20” in the direc-

tion of that stimulus. The time spent over the defined ori-

entation sectors was recorded with the internal clock of

the compu ter through the Observer sofware (Noldu s Infor-

mation Techn ologies, Wageningen, The Netherlands)

with an accuracy of 0.1 s. The total time oriented to either

stimulus was obtained by adding the different orientation

durations recorded accross the two consecutive trials. The

orientation duration toward a given stimulus is reported

as the mean proportion of time sp ent toward that ss in

function of the total time of orientation (120 s) to either ss

and to either sfs. Interobserver agreement for orientation

durations to the ss and sfs calculated by two coders una-

ware of the nature of the stimuli presented was highly

significan t (all Spearman rank-order correlation coeffi-

cients: r > 0.95, n = 20).

Results

A two-way ANOVA, with odour as the within-subject fac-

tor and age/feeding experience group as the between-sub-

ject factor, yielded significan t main effects of odour

(F(1,61) = 402.5, P < 0.0001) and of age/feeding expe-

rience group (F(4,61) = 5.69, P < 0.001 ), and a significan t

odour x group interaction (F(4,61) = 5.72, P < 0.001). The

time course of the relative response in the two-choice test

is presented in

figure

I for the different groups. Within-

group comparisons of relative orientation duration indi-

cate that groups l-3 do not orient significantly longer to

the AF odour than to the lacteal (L) odour (cf. table I). In

contrast, groups 4 and 5 orient longer to the odour of milk

than to the odour of AF (cf. tab/e I). Thus, after 7-l 2 breast

feeds within 72 h of life, newborns display an average pre-

ference for the odour of their mother’s milk when it is pre-

sented along with the odour of their own AF.

It is notable that the stimulus bearing the lacteal odour

elicits steadily increasing head-orientation durations as a

function of age/feeding experience, while the orientation

response toward AF remains stable for the first 3 days,

and then decline s over the following 2 days (figure 7).

Between-group comparisons indicate heterogeneity of

orientation duration to AF throughout the 1-5-day period

(f (4,61) = 3.68, P < O.Ol), with a significan t decrease in

attraction to AF odour between days 2 and 5 (P < 0.05,

post-hoc Tukey test). In contrast, between-group compar-

isons on the orientation duration to the lacteal odour indi-

cate a significan t increase in attraction to this odour

between days 1 and 5 (F (4,61) = 5.7, P < 0.001). Signif-

icant rises in orientation to the lacteal odour are situated

between group 1 and groups 4 and 5, and between

group 2 and group 5 (P < 0.05, post-hoc Tukey tests).

The choice pattern of individual infants was further

examined by comparing the number of subjec ts spending

longer oriented toward one stimulus than toward the

other. Infants were defined as orienting longer to one stim-

ulus than to the other when they spent more than 50 of

the total orientation time to both stimulus sectors turned

.toward that stimulus . From groups 1-5, respectively 2 on

9 (22 %I, 8 on 20 (40 ), 6 on 12 (50 %), 13 on 16

(81.25 ) and 8 on 9 subjects (88.89 ) oriented longer

1002

C. R. Acad. Sci. Paris, Scienc es de la vie / Life Scien ces

1997.320,999-1005


5/7

Mean relatlue dumtbn

097

096

0,s

0,4

013

092

091

0

*

Groups 1 2 3 4 5

Figure 1. Mean relative durations (i confidence intervals at 5

risk) of head orientation of five groups of breast-feeding infants of

different ages exposed to choice tests opposing simultaneously an

odour from the prenatal environment (amniotic fluid: Af; hatched

columns) and an odour from the postnatal environment (maternal

lacteal secretions: L; black columns).

For fhe number of subjects , range of age and of breast-feeding expe-

rience in each group, see table I. Intra-group differences in orienta-

tion duration: ” P < 0.0 1.

to the odour of their mother’s lacteal secretion than to AF

odour (x2 = 14.47, df = 4, P < 0.01). The percentage of

subjec ts orienting more to the lacteal odour than to the AF

odour is not statistically different in groups 1, 2 and 3, but

it is between these groups and groups 4 and 5 (groups l-

4: x2 = 8.36; groups l-5: x2 = 8.10; groups 2-4: x2 = 6.22;

groups 2-5: x2 = 6.0; in all cases , P < 0.02; groups 3-4:

x2 = 3.07, P = 0.07; groups 3-5: x2 = 3.5; P = 0.06;

x2 tests;

in all cases , df = 1).

Discussion

This study reveals a biphas ic time course of relative prefe-

rence of breast-fed newborns between two biologically

relevant odours experienced either prenatally or postna-

tally in assoc iation with ingestion. On days l-3, the

infants do not show evidence of a reliable differentiation

of both odours. This outcome may result from their lack of

ability to either i) detect the low intensity odours carried

in biologic al fluids, ii) discriminate them on chemosen-

C. R. Acad. Sci. Paris, Sciences de la vie / Life Sciences

1997. 320, ‘X9-1005

Plasticity

of odour

responses

in the human newborn

sory basis, or iii) discriminate them on hedonic basis. Pre-

vious experiments demonstrated clear detection a bilities

of the faint odour borne in biologic al substrates in new-

borns soon after birth [9, 10, 161. As both other alternati-

ves cannot be singled out with the present experimental

paradigm, we will consider parsimoniously that the sub-

jects tend to process amniotic and lacteal odours as che-

mosensorily and/or hedonically similar before and on

postnatal day 3.

However, with both increasing age and exposure to

feeding cues, infants display greater attraction to their

mother’s lacteal odour than to their own AF odour. A

steady increase in relative orientation length to lacteal

odour ca n be observed throughout the 5-day period cov-

ered by the present study, but it differentiates significantly

from the attraction duration toward the AF odour after the

3rd day. Thus, our results suggest that some s pecia l events

might occur after the 3rd postnatal day to modify the bal-

ance of relative response between AF and lacteal odours.

Several processes may be involved in the sequential

development of relative preference behaviour evidenced

by the two-choice test. i) The motor constraint associated

with the head-turning task might exceed the newborns’

abilities during the first 3 days after birth. It cannot be

excluded that the recording of less demanding responses,

such as oral or vocal activities, or state changes, would

bring about an earlier disc rimination ability of both types

of odours. However, hour-old newborns were capable of

expressing directional head turning and focused crawling

responses in a much more demanding situation (in which

they were laid prone on their mother’s chest midline in

order to reach a nipple without any assistan ce [l 11). Thus,

age-increasing motor capab ilities do not adequately

explain the observed pattern of preference development.

ii) The nasal chemosensory system of the human newborn

may have to reach a certain level of maturation to support

fine-grained discrimination of odour qualities. Earlier

investigators have demonstrated, however, that olfactory

discrimination can operate from the day of birth in term

newborns [I 7, 181, and that preterm newborns already

show evidence of differential responses to different odour

qualities [19]. iii) The neonatal brain may have to inte-

grate a certain level of exposure with a ‘novel’ odour to

positively respond to it and to overcome the prenatally

acquired positive response to AF odour. The above data

would suggest that, on average, more than 7-l 2 nursing

episodes might be necessary within the first 3 days for the

infant to become sensitized or familiarized with the odour

of milk, and to perceive lacteal odour as different from, or

more strongly reinforcing than, AF odour. However, one

study indicates that newborns exposed to an arbitrarily

selected artificial odour in associa tion with breast feeding

display evidence of conditioned responses in favour of

that odour 2 h after only one acquisition sessio n [201. Fur-

thermore, ‘mere’ exposure to an artificial odour without

associa tion with feeding has been suggested to later elicit

attraction responses [18]. Thus, the accumu lation of expe-

1003


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L. Marlier et al.

rience with lac teal odour in the feeding context does not

fully explain the relative preference for milk odour emerg-

ing after daly 3. iv) An additional process may involve a

progressive change in the quality of milk which facilitates

the differentiation of its odour from that of AF. As tran-

sudates of maternal plasma, both fluids have overlaping

compo sitions majorly influenced by the aromas of the

mother’s diet. Thus, amniotic and lacteal fluids should

share a high degree of similarity during the initial colostral

phase, when their aromatic profiles are elaborated under

the synchronous influence of exogenous aromas. Th is

degree of similarity decreases then during the first post-

partum days, and especially after day 3 with the inception

of lactogene sis [14, 21, 221. Accordingly, the olfactory

discrimination of amniotic and lacteal fluids is easier in

newborns aged more than 3 days. Finally, v) the rise of rel-

ative attraction to the lacteal odour may be explained in

terms of growing avoidance of AF odour. The reduction in

attractiveness of AF odour is most apparent after day 3.

Previous choice tests contrasting AF odour with a control

stimulus inclicat e that AF odour does not become aversive

after day 3, however [9]. This reduction may rather reflect

a process of conditioned extinction of AF odour associ-

ated with the decrease in re-exposure to AF-like odour

cues carriecl in lacteal secretions, and repetition of expo-

sure to novel cues in lacteal odors.

The progressively divergent orientation response curves

to either odours may reveal the action of two concurrent

processes involving learning in the perinate. The initial

stage (days l-3 and up to 7-l 2 feeds) may reflect the new-

borns’ use of an odour template derived from their expe-

rience with AF and the quasi-similar sensory or

motivational treatment of AF and lacteal odours. The sec-

ond stage (days 4-5 and more than 12 feeds) may reflect

the infants’ perception of chemosensory change in milk

quality and the sharpening of milk odour with increasing

exposure time to it. This sequential development attests

for a high level of functional plasticity in the initial stages

of olfactory development in the human perinate, as was

previously described in animal newborns [23, 241. It is

worthwhile to underline that this notion of perinatal olfac-

tory plasticity is enrooted in the ability of the human fetus

to encode odour information from its amniotic environ-

ment, and to retain and us e it transnatally.

Conclusion

This study reveals that human newborns may be anticipa-

torily adjusted to the chemosensory qualities of colostrum

through their experience with similar qualities in utero,

and that by age and feeding experience they re-adjust to

the progressive change in lacteal chemosensory proper-

ties occurring with lactogenesis onset. A s in other mam-

malian newborns [3, 5, 7, 8, 23, 241, human newborns

may be born with chemosensory images that direct the

initial expression of attraction or withdrawal when they

are confronted with biologica l odour s timuli in the pos-

tamniotic environment. The procedure used here does not

allow us to separate the relative contributions of age and

feeding experience in the development of the positive res-

ponse to lacteal odours. An ongoing longitudinal study

should allow us to separate the effects of both factors in

testing same-age children differing in their spontaneous

amount of breast-feeding experience.

Acknowledgments: This work was supported by grant R96/07 from Direction g&n&ale de I’Alimentation. ministere de I’Agriculture

(to BS and RI;), and a fellowship from Danone Institute (to LM). We are indebted to the direction, midwives, nurses and technic ians

of the clinique Sainte-Anne, Strasbourg, for their help throughout the study, and to the parents, for letting their infants participate

in the study.

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