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0 Academic

Neurosciences

des sciences / Elsevier,


/ Neurosciences

Paris

Orientation
responses to biological odours
in the human newborn. Initial pattern
and postnatal plasticity
Les r6ponses dorientation
aux odeurs biologiques
chez le nouveau-n6
hurnain. itat initial et plasticit

Laboratoire

depsychopbysique

2 Laboratoire

de comportement

sensorielle,
animal,

CNRS

CNRS

EP 618,

universitP

URA 1291 et station

3 Dkpartement
de psycbologie, universiti
de Reims, et laboratoire
41, rue Gay-Lussac,
75006 Paris, France

Lou&Pasteh,
dephysiologie

de psychobiologie

IO. rue Goethe,


de la reproduction,

Strasbourg,

67000

Inra,

du developpement,

37380

&ole pratique

Les rtponses initiales dorientation


et leur developpement
precoce sont analysees chez des
nouveau-nts exposes simultanCment a Iodeur de leur liquide amniotique
(AF) et a lodeur des
secretions lactees (L) maternelles. Lorientation
relative entre ces deux odeurs est etudiee en fonction de lhge postnatal (1-5 j) et de lexperience 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
dequivalence sensorielle et/au hedonique dAF 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 lexposition repetee a lodeur L et un changement
qualitatif du lait maternel lors de linstallation de la lactogenese. Cette sequence dkeloppementale
rhele que : i) les reponses du nouveau-m? humain au colostrum pourraient etre influencees par
lexposition 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&
plasticit

: nouveau-n&
comportementale,

humuin.
fcefus,
naissance.

olfaction,
adaptation

liquide
amniotique,
neonatale

colosfrum.

lait maternel,

ABSTRACT
The initialpa.ttern

and development

of odourpreference

was studied

in infants

simultaneously

to amnioticfltrid
(AF) and maternal
lactealsecretion
(L). Fivegroups
of varying
were studied.
Before postnatal
and breast-feeding
experience
(range: S3.2 fee&)
differentiation
ofAF and L was apparent.
AjZer 3 days and 7-12
breast-feeding
preference
for L arised.
The initial
stage (days 1-3)
may reflect fetal acquisition
sensory/motivational
equivalence
of AF and L odours.
The second stage (days
infantsperctption
of change in milk
development
attests to a high plasticity
Key words:
behavioural

human
plasticity,

and

accept&

aprks

r&i&n

le 17 novembre

reprints

C. R. Acad. Sci. Paris, Sciences


1997. 320.999-1005

exposed

age (range:
I-5 day)
c&y 3, no evidence of
episodes, a rignQ%ant
of AF odour and
4-5)
may reflect
the

increasing
experience
with milk.
This
stage of human
o/facto y development.

newborn,
human
fetus,
olfaction,
birth, neonatal
adaptation

Note prbentte
par Pierre Ruser
Note remise le 15 septembre
1997,
*Correspondence

quality
and
in the initial

de la vie / Life Sciences

amniotic

1997

fluid,

colostrum,

sequential

breast

postnatale

milk,

France

Not&l&

France

des bautes Jtudes,

L. Marlier

et al.

VERSIONABR&EII?
Chez pluskurs esptces de mammiferes placentaires, la s&ctivitk des rkponses nkonatales envers Ies stimulations olfactives apparair dkpendante
de lexptrience
olfactive fcetale.
Linformation
olfactive acquise in utero conscitue ainsi une
solution de continuitk sensorielle lors de la transition natale.
Une telle continuitC olfactive transnatale a kte sugg&e dans
le cas de lespkce humaine. Des enfants ?I& de 2 j, nourris au
sein, nexpriment
pas de reponse dorientation
dphalique
diffkrentielle dans un test de double-choix
olfactif prtsentant
simultan&ment lodeur de leur liquide amniotique et lodeur
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 Ialimentation maternelle dans les compartiments
fcetal et mammaire.
Cette etude ;apour but dexaminer deux prtdictions qui d&ivent de lhypothkse de continuitk chimiosensorielie
transnatale :
i) Le de@ (de similarice chimiosensorielle
des deux fluides
devrait Ctre maximal peu aprks la naissance, lorsquils sont
soumis g linfluence simultanee du profil aromatique de la
dikte maternelle. Cette similarit
plus marquke entre les
odeurs amniotique
et colostrale devrait alors rksulter en
labsence 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 lexpkrience de t&e au sein ; en
particulier, la direction des reponses devrait Ctre mod&&e B la
fin de Ia phase colostrale, lorsque la qualiti aromatique des
s&r&ions la&es est radicalement modifiee du fait de linstallation des mkanismes galactopokkiques.
Ces deux hypothkses sont examinkes dans une Crude transversale de nouveau-n& Sg& de 5 h B 5 j et dont lexposition 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 doublechoix olfactif. Leurs caractkristiques d%ge et dexpbrience alimentaire 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 dune quantitC tquivalente des sCcr&ions 1actCes
maternelles (L). Ces stimulations sont prksenttes de part et
dautre du visage de lenfant, 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 effets potentiels
dune 1atCralisation motrice ou sensorielle, chaque sujet est
tgalement expose aux deux stimulations g droite et a gauche.
Les tests sont video-enregistrks
et lanalyse des rkponses est
r&Me
par un dkcodeur aveugle quant au c&C de prksentation des stimulations.
Les dukes dorientation
vers lun et
iautre stimulus sont mesukes a laide du logiciel Observer.
Le crittre dorientation
vers un stimulus est atteint lorsquun

1000

sujer positionne son nez au-dessus du stimulus, ce qui n&essite une dCviation minimale de 20 par rapport au plan sagittal. La duree dorientation
vers un stimulus est donnee
comme la proportion
moyenne du temps dorientation
vers
ce stimulus en fonction du temps total dorientation
(120 s.).
Le d&ours temporel des rkponses dorientation
relative dans
les tests de choix est present& dam la$pre
1. Une analyse de
variance a deux facteurs (nature de Iodeur et groupe dSge/
experience de t&t&e) rkvkle des effets principaux de lodeur
@ < 0,000 1) et du groupe (p < O,OOl), et une interaction
signifkative entre lodeur et le groupe (p < 0,001). Des comparaisons intragroupes indiquent que les durkes dorientation
relative entre AF et L ne different pas dans les groupes 1 ?I 3
(tableau Z). Les groupes 4 et 5 sorientent plus longuement
vers lodeur L que vers lodeur AF (tableau I). Les nouveaun& manifestent une prkfkrence moyenne B lkgard de lodeur
de L aprks 72 h de vie et 7-12 episodes de tCtCes. Des comparaisons intergroupes r&&lent une dtcroissance de la durke
dorientation
vers lodeur AF et, surtout, un accroissement
rkgulier de la duke dorientation
vers lodeur L. Cet accroissement vers Iodeur L est signifkatifentre
les groupes 1 et 2 et
les groupes 4 et 5.
Cette etude met en hidenceun
d&ours temporel biphasique
de lorientation
relative des nouveau-n& vers deux substrats
odorants auxquels ils ont ttt exposks avant ou aprb la naissance. Au tours des jours postnatals 1 B 3, les enfants nexpriment aucune diffkrenciation
sensorielle ou hCdonique
significative des deux stimularions. Cependant, en fonction
de 1Sge et de lexpkrience de tCtke, les enfants manifestent
une attraction plus grande vers lodeur L que vers lodeur 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
laction de deux processus synergiques. La premike phase
(jours 1-3 et O-12 tCt&.s) semble refker, dune part, une
rPponse prefdrentielle du nouveau-&
?I legard dune information acquise B lktat fcetal, lodeur du liquide amniotique,
et dautre 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 dune modification
qualitative
de
lodeur du lait ; aprks linstallation
de la lactation, lodeur des
s&r&ions lacttes dhierait
de faGon croissante de celle du
colostrum, rendant la discrimination
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 lexprkience nionatale. Les rCponses du nouveau-nt humain au colostrum pourraient Ctre influendes par
lexposition
g des qualit& chimiosensorielles
similaires in
utero, et elles sajustent au changement progressif des propritt&s chimiosensorielles
du lait qui interviennent
avec la
lactogenkse.

C. R. Acad.

Sci. Paris, Sciences

de

la vie / Life Sciences


1997. 320.999-1005

Plasticity

Introduction
The

successful

transition

from

the amniotic

with
early

behavioural
developmental

and

to the postam-

cognitive
capabilities
adjustments
[l].

hours
after birth,
they learn
how
ple,
and
to obtain
milk.
Their
obviously
vital
tasks
is rapidly

that
Within

to find and seize a nipperformance


in these
improved
and attuned

[2]. The
imprints

fetal brain
has
and coordinated

vioural
training
[3]. The experience-based
med in utero
has been shown
to serve
very
first suc:king
episodes
in the rat

postnatal
colostrum.

human

newborn

no or very
limited
sucking
of such very young,
feedthe primal
stage of relative

exposure
Second,

to AF-like
the initially

cues potentially
similar
treatment

carried
in
of both

fluids
is expected
to change
with
both
age and feeding
experience,
in the same time that colostrum
is progressively
transformed
into milk with the advent
of lactogenesis.
These
two
hypotheses
were
examined
in
a
developmental,
cross-sectional
study
involving
breast-fed

already
beha-

plasticity
the success
[3-51.
Thus,

in the

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

through
the experience
gained
from their earlier
realization.
Thus,
learning
and underlying
neural
plasticity
are
essential
components
of the adaptation
to the postnatal
niche.
However,
the integrative
activity
of the brain is not
initiated
sharply
at birth
been exposed
to sensory

responses

ducted
with newborns
having
experience.
The responsiveness
ing-naive
infants,
should
settle

niotic
niche
requires
numerous
adaptations
in newborn
mammals.
Besides
the well-documented
cardio-vascular,
respiratory
and
gastro-intestinal
adaptations,
they
are
endowed
optimize

of odour

newborns
exposure

forof the
odour

aged from
5 h to 5 days and
to milk
ranged
from
0 to 32

whose
breast

amount
feeds.

of

information
gained
in the amniotic
atmosphere
constitutes a tie of familiarity
bridging
the fetal and the neonatal
niches
in this species.
The relationship
of fetal learning
to
neonatal
adaptation
and learning
has been investigated
in

Subjects and methods

other
species,
and humans

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
ingestive experience
and age at the moment
of the choice
tests.
The number
of subjects,
age and feeding
experience
cha-

Human
suggested
response

including
[9-l I].

mice

[6],

rabbits

[7]

sheep

Subjects

181,

evidence
of perinata]
olfactory
continuity
was
in a recent
report
on the undiscriminative
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 undifferentiated
olfactory
response
has been
hypothesized
to

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
subjects
had only
limited

reflect
similarity
simultaneous
mother
into

sucking
experience
in the delivery
room.
Mothers
provided informed
written
consent
to let their
infants
participate in the tests. Each subject
was tested
only once.

112,

of both
perinatal
substrates
due to the
transfer
of the aromas
ingested
by the
the
fetal
and
mammary
compartments

131.

If this
forecasts
sensory
partum

chemosensory

continuity

two expectations.
similarity
of AF and
mammary
secretion

hypothesis

First, the degree


colostrum
(also
[141)
should

around
birth when
both fluids
temporaneous
priming
of the
This greater
AF/colostrum
odour
an

absence

Table
tions
lacteal

of

relative

is correct,

Stimuli

it

Two types
of stimulations
of blood
or meconium

of chemonamed
prebe highest

in

1. The characteristics
(number,
age,
[means
(M) and standart
deviations
secretions.

choice

feeding
(s.d.)l

tests

test.

con-

experience)
when
exposed

of the five
concurrently

groups

Both

types

of newborns
to the odours

Relative
Groups

Age

N subjects
M

s.d.

9.67

Feeding-experience
range
(N feeds)

(hi

used. AF samples
devoid
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

are submitted
to the conmothers
dietary
aromas.
similarity
should
result in

preference

were
staining

range

of stimulations

studied
of their

orientation

were

and their
relative
familiar
amniotic

presented

head-orientation
fluid
and their

duration

(s)

Lacteal

Fluid

Amniotic

Fluid

s.d.

s.d

at room

duramothers

t*

4.12

515

o-1

0.368

0.205

0.239

0.127

1.62

NS

2
3

20
12

33.6
55.42

8.16
8.48

22118
49-72

2-6
7-l

0.382
0.325

0.171
0.141

0.330
0.388

0.187
0.115

0.68
0.99

NS
NS

4
5

16
9

85.06
114.22

7.91
11.79

0.221
0.193

0.148
0.137

0.43 1
0.537

0.136
0.108

3.3
4.6

0.004
0.002

C. R. Acad.
Sci. Paris,
1997. 320,999.1005

Sciences

de

la vie

7>95
96-l
40

/ Life

Sciences

13-19
>20

L. Morlier

et CII

temperature

on

10 x 10

cm

Hartmann,
Chstenois,
France).
substrate
used in the paired
prior
ratings
of the intensity
panel

gauze

pads

(100

% cotton,

The equal amount


of each
odour
tests was fixed
after
of their
odour
by an adult

[9].

Apparatus
When

arousal

were
installed
at a 25 angle

state

3-4

[I51

was

in a semi-reclining
with the vertical.

obtained,

the

infants

seat which
back was set
Both stimulus
pads were

fastened
on an U-shaped
device
that allowed
us to present 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
possible
trajectory
of the infants
nose. The infants
visual
scene was homogenized
by spreading
a sheet all around

mation
Technologies,
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
spent 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
unaware
of the nature
of the stimuli
significant
(all Spearman
rank-order
cients:
r > 0.95,
n = 20).

presented
was
correlation

highly
coeffi-

Results
A two-way

ANOVA,

with

odour

as the within-subject

fac-

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.

tor and age/feeding


experience
group
as the between-subject
factor,
yielded
significant
main
effects
of odour
(F(1,61)
= 402.5,
P < 0.0001)
and of age/feeding
experience
group
(F(4,61)
= 5.69,
P < 0.001 ), and a significant

Procedure
After the stiimuli
were
positioned
symmetrically
on each
side of the infants
head,
the experimenter
(who
stood
behind
the infant)
manually
turned
the infants
head
in

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.
Withingroup
comparisons
of relative
orientation
duration
indi-

order
to alternately
orient
their nose to each stimulus
pad
for 5 s. The direction
of this pretest
orientation
was systematically
counterbalanced
for the nature
and lateral
position of the first stimulus
presented.
The infants
head was

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

then returned
to the sagittal
position
dissipation
of tonic
neck
asymmetry.

feeds within
72 h of life, newborns
display
an average
preference
for the odour
of their mothers
milk when
it is presented
along with the odour
of their own AF.

and released
after
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 presented
from the left side, and vice versa. The infants
head

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

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-

response
toward
AF remains
and
then declines
over the
Between-group
comparisons

muli was controlled


equally
often
from
within
and between

orientation
(f (4,61)

so that both
the right
or
subjects.

stimuli
were
from
the left

presented
side both

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 possible
trajectory
of
180
three

that the
angular

newborns
sectors

nose could
on each side

scan was divided


into
of the infants
head:
a

stable
for the first 3 days,
following
2 days (figure
7).
indicate
heterogeneity
of

duration
to AF throughout
the 1-5-day
period
= 3.68,
P < O.Ol),
with a significant
decrease
in

attraction
to AF odour
between
days 2 and 5 (P < 0.05,
post-hoc
Tukey
test). In contrast,
between-group
comparisons on the orientation
duration
to the lacteal
odour
indicate
a significant
increase
in attraction
to this
odour
between
days 1 and 5 (F (4,61)
= 5.7, P < 0.001).
Significant rises in orientation
to the lacteal
odour
are situated
between
group
1 and groups
4 and
5, and between

sector
corresponding
with the stimulus
(labelled
stimulus
sector,
ss), and two sectors
corresponding
with the zones
free of stimulus
(covering
the o-20
and 70-90
angles

group

with the infants


sagittal
plane;
labelled
stimulus-free
sectors,
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-

longer
oriented
toward
one stimulus
than
toward
the
other.
Infants
were defined
as orienting
longer to one stimulus 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

tion of that stimulus.


entation
sectors
was
the computer
through

1002

The time spent over the defined


orirecorded
with
the internal
clock
of
the Observer
sofware
(Noldus
Infor-

2 and

group

5 (P < 0.05,

The choice
pattern
examined
by comparing

9 (22
(81.25

of

post-hoc

individual
the number

%I, 8 on 20
%) and

Tukey

(40 %), 6 on 12 (50 %),


8 on 9 subjects
(88.89
%) oriented

C. R. Acad.

Sci. Paris, Sciences

tests).

infants
was further
of subjects
spending

13 on

16

longer

de la vie / Life Sciences


1997.320,999-1005

Plasticity

newborn

0,s

mosensorily
postnatal

0,4

However,
with
both
increasing
age and exposure
to
feeding
cues,
infants
display
greater
attraction
to their
mothers
lacteal
odour
than
to their
own
AF odour.
A
steady
increase
in relative
orientation
length
to lacteal

might
ance

Groups

1. Mean

relative

durations

risk) of head orientation


different
ages exposed
odour
from the prenatal

(i

hedonically

similar

before

and

on

occur
after the 3rd
of relative
response

postnatal
between

day to modify
AF and lacteal

For fhe number


rience
in each

of subjects,
group,
see

tion

P < 0.0 1.

duration:

to the odour

of their

range
of age and
table
I. Intra-group

mothers

intervals

at 5 %

of breast-feeding
infants
of
opposing
simultaneously
an
(amniotic
fluid:
Af; hatched
environment

lacteal

(maternal

of breast-feeding
expedifferences
in orienta-

secretion

than

to AF

odour
(x2 = 14.47,
df = 4, P < 0.01).
The percentage
of
subjects
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
l4: x2 = 8.36; groups
l-5:
x2 = 8.10; groups
2-4: x2 = 6.22;
groups
2-5:
x2 = 3.07,

x2 = 6.0;
P = 0.07;

in all

cases,

in all cases, P < 0.02;


groups
groups
3-5:
x2 = 3.5; P =

3-4:
0.06;

df = 1).

Discussion
reveals

a biphasic

time

course

of relative

prefe-

rence
of breast-fed
newborns
between
two biologically
relevant
odours
experienced
either
prenatally
or postnatally
in association
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
in biological
fluids,
ii) discriminate
Sci. Paris,
X9-1005

Sciences

de

intensity
them

la vie

/ Life

odours
carried
on chemosenSciences

the balodours.
sequential
evidenced
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
discrimination
ability
of both types

confidence

of five groups
to choice
tests
environment

and an odour
from the postnatal
secretions:
L; black
columns).

study

and/or
3.

Several
processes
may
be involved
in the
development
of relative
preference
behaviour
by the two-choice
test. i) The motor
constraint

x2 tests;

day

odour
can be observed
throughout
the 5-day
period
covered 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 special
events

091

C. R. Acad.
1997. 320,

human

096

092

This

in the

borns soon after birth


[9, 10, 161. As both other
alternatives cannot
be singled
out with the present
experimental
paradigm,
we will consider
parsimoniously
that the subjects tend to process
amniotic
and lacteal
odours
as che-

013

columns)
lacteal

responses

sory basis, or iii) discriminate


them on hedonic
basis. Previous
experiments
demonstrated
clear detection
abilities
of the faint odour
borne
in biological
substrates
in new-

Mean relatlue dumtbn


097

Figure

of odour

of odours.
expressing
responses
they were

However,
directional
in a much
laid prone

hour-old
newborns
were capable
of
head turning
and focused
crawling
more demanding
situation
(in which
on their
mothers
chest
midline
in

order to reach a nipple


without
any assistance
[l 11). Thus,
age-increasing
motor
capabilities
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
show evidence
of differential
responses
qualities
[19].
iii) The neonatal
brain
grate a certain
level of exposure
with

newborns
already
to different
odour
may have to intea 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 association
with breast feeding
display
evidence
of conditioned
responses
in favour
of
that odour
2 h after only one acquisition
session
[201. Furthermore,
mere
exposure
to an artificial
odour
without
association
attraction

with feeding
has been suggested
to later elicit
responses
[18]. Thus, the accumulation
of expe-

1003

L. Marlier

et al.

rience
with
fully explain

lacteal
odour
in the feeding
context
does not
the relative
preference
for milk odour
emerg-

ing after
progressive

3. iv) An additional
change
in the quality

daly

process
may
of milk which

involve
facilitates

ond
the
a

the differentiation
of its odour
from
that of AF. As transudates
of maternal
plasma,
both fluids
have overlaping
compositions
majorly
influenced
by the aromas
of the
mothers
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.
This
degree
partum

of similarity
decreases
then during
days, and especially
after day 3 with
221. Accordingly,
and lacteal

[14, 21,
of amniotic

newborns
aged
ative attraction
terms of growing

more than 3 days. Finally,


v) the rise of relto the lacteal
odour
may be explained
in
avoidance
of AF odour.
The reduction
in

the
fluids

olfactory
is easier

in

after day 3.
with a control

stimulus
inclicate
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
associated
cues

with
the decrease
carriecl
in lacteal

sure

to novel

The

cues

progressively

to either
processes

in re-exposure
secretions,
and

in lacteal
divergent

odours
may reveal
involving
learning

to AF-like
odour
repetition
of expo-

odors.
orientation

response

the action
of two
in the perinate.

curves

concurrent
The initial

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


the newborns
use of an odour
template
derived
from their experience
with
AF
and
the
quasi-similar
sensory
or
motivational

treatment

of AF and

lacteal

odours.

Acknowledgments:
This work was supported
by grant
(to BS and RI;), and a fellowship
from Danone
Institute
of the clinique
Sainte-Anne,
Strasbourg,
for their help
in the study.

The

sec-

and

more than 12 feeds)


may reflect
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
olfactory plasticity
is enrooted
in the ability
of the human
fetus
to encode
odour
information
from
its amniotic
environment,
and to retain
and use it transnatally.

Conclusion
This study reveals
that human
newborns
may be anticipatorily
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
properties occurring
with
lactogenesis
onset.
As in other
mammalian
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
biological
odour
stimuli
in the postamniotic
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
response
to lacteal
odours.
An ongoing
longitudinal
study
should
testing
amount

allow
us to separate
the effects
of both factors
same-age
children
differing
in their
spontaneous
of breast-feeding
experience.

in

R96/07 from Direction


g&n&ale
de IAlimentation.
ministere
de IAgriculture
(to LM). We are indebted
to the direction,
midwives,
nurses and technicians
throughout
the study, and to the parents,
for letting their infants participate

REFERENC:ES
1. Alberts J.A. 1987. Early learning
and ontogenetic
adaptation.
In: Perinatul Development:
A Psychobiological
Perspective
(Krasnegor
N.A.. Blass E.M.. Hofer M.A., Smotherman
W.S.. eds.),
Academic
Press, Orlando,
11-37
2. Lecanuet
J.P., Fifer W.P.. Krasnegor
N.A., Smotherman
W.P.
(eds.) 1995. Fetal Development: A Psychobiological Perspective.
Lawrence
Erlbaum,
Hillsdale
3. Smotherman
W.P., Robinson
S.R. 1988. The uterus as environment: The ecology
of fetal behavior.
In: Handbook
ofEehuvioru/

Neurobiology, Vol. 9, Developmental Psychobiology and Behavioru/Eco/ogy(Blass E.M.. ed.), Plenum, New York, 149-196
4. Teicher M.H.. Blass EM 1977. First suckling response
in the newborn albino rat: the roles of olfaction
and amniotic
fluid. Science
198,635~636
5. Smotherman
W.P., Robinson
S.R. 1995. Tracing developmental
trajectories
into the prenatal
period.
In: Fetal Development: A
PsychobiologicalPerspective
(Lecanuet
J.P., Fifer W.P., Krasnegor
N.A., Smotherman
W.P., eds.), Lawrence
Erlbaum,
Hillsdale. 15-32

1004

(days 4-5
perception

the first postthe inception

of lactogenesis
discrimination

attractiveness
of AF odour
is most apparent
Previous
choice
tests contrasting
AF odour

stage
infants

6. Coppola
D.M.. Millar L.C. 1997. Olfaction
in utero: behavioral
studies of the mouse fetus. Behav. Processes 39,53-48
7. Bilko A., Altbticker
V., Hudson R. 1994. Transmission
of food preference
in the rabbit: the means of information
transfer.
Physiol.

Behav. 56,907-912
8. Schaal B.. Orgeur
P., Arnould C. 1995. Chemosensory
preferences in newborn
lambs: prenatal
and perinatal
determinants.
Behuviour 132.352-365
9. Marlier L.. Schaal B.. Soussignan
R. (in press). Neonatal
responsiveness to the odour of amniotic
and lacteal fluids: a test of perinatal chemosensory
continuity
Child Develop.
10. Schaal B.. Marlier L.. Soussignan
R. 1995. Responsiveness
to the
odor of amniotic
fluid in the human
neonate.
Viol. Neonate
67.
397-406
11, Varendi H.. Porter R., Winberg
J. 1996. Attractiveness
of amniotic fluid odor: evidence
of prenatal
learning?
Acta faediatr.
85,
1223-1227
12. Mennella
J.A., Johnson
A., Beauchamp
ingestion
by pregnant
women
alters the odor
Chem. Senses 20,207.209
C. R. Acad.

Sci. Paris, Sciences

G.K. 1995.
of amniotic

Garlic
fluid.

de la vie / Life Sciences


1997.320.999-1005

Plasticity
13. Mennella
.J.A., Beauchamp
G.K. 1996. The human infants responses to vanilla flavors in human milk and formula.
Infant Behav.
Develop.
19, 13-19
14. Neville M.C. 1995. Lactogenesis
in women:
A cascade
of
events
revealed
by milk composition.
In: Handbook
of Milk
Composition
(Jensen
R.G., ed.), Academic
Press, San Diego,
CA, 07-98
15. Prechtl
H.F.R. 1974. The behavioral
Infant - A review. Bruin Res. 76, 185-2 12

states

of the

newborn

16. Soussignan
R., Schaal B., Marlier
L.. Jiang T. 1997. Facial and
autonomic
responses to biological
and artificial olfatory
stimuli in
human
neonates:
Re-examining
early hedonic
discrimination.
Physiol. Behav. 62, 745-758
17. Steiner J.E. 1979. Human facial expressions
in response to taste
and smell stimulations.
In: Advances
in Child Development,
Vol. 13
(Lipsitt L.P., Reese H.W., eds.), Academic
Press, New York, 257-295
18. Balogh R.D., Porter R.H. 1986. Olfactory
from mere exposure
in human neonates.
9,395-40
1

C. R. Acad. Sci. Paris, Sciences


1997.320,999-1005

preferences
infant Behav.

de la vie / Life Sciences

resulting
Develop.

of odour

responses

in the human

newborn

19. Pihet S., Mellier D.. Bullinger A., Schaal B. 1997. Reponses
comportementales
aux odeurs
chez
le nouveau-&
premature:
etude preliminaire.
Enfance
1 /1997,33-46
20. Sullivan R.M. 1990. Newborn
human infants exhibit CRs to an
odor previously
paired with either breast od bottle feeding.
Presented at the Annual Meeting
of Intern. Sot. Devel. Psychobiol.,
Cambridge,
UK
21. Kulski J.K., Harmann
P.E. 1981. Changes
in milk composition
during
initiation
of lactation.
Au&r. J. Exp. Biol. Med.
Sci. 59.
101-l 10
22. Patton
S., Huston GE,
Montgomery
P.A., Josephson
R.V.
1986. Approaches
to the study of colostrum
-The onset of lactation In: Humun
Lactation
2, Maternal
and Environmental
Factors (Hamosh
M., Goldman
AS. eds.), Plenum Press, New York,
231-238
23. Hudson R. 1993. Olfactory
imprinting.
Curr Opin. Neurobiol.
3.
548-552
24. Wilson D.A., Sullivan R.M. 1994. Neurobiology
of associative
learning
in the neonate:Early
olfactory
learning.
Behov. Neural
Biol. 61, l-l

1005