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Olfactory responsiveness was assessed in 24 neonates born to mothers who had or had not consumed anise flavour during pregnancy.
Both groups of infants were followed-up for behavioural markers of attraction and aversion when exposed to anise dise and a control odour immediately after birth and on day 4. Infants born to anise-consuming mothers evinced a stable preference for anise odour over this period, whereas those born to anise kkehl mothers displayed aversion or neutral responses.
The findings have potential implications for the early mother-to-infant transmission of chemosensory information relative to food and addictive products. During the embryonic or foetal stages, the environment constrains the perceptual information available to the growing brain and thus influences the behaviour of the newborn Smotherman and Robinson, ; Lecanuet et al. In humans, for example, the way vocal and speech sounds are processed by the newborn depends on prenatal exposure to maternal voice or specific speech sequences De Casper and Spence, ; Fifer and Moon, Whether this foetal ability is indicative of mechanisms specific to audition and language processing or of more general learning mechanisms applicable to a broad range of perceptual inputs remains unclear.
We investigated whether the human foetus can acquire information from olfactory cues, which are involved in other psychobiological realms such as ingestive behaviour, emotional stability and early attachment Schaal, The ability to learn olfactory cues has been demonstrated in the foetuses of various mammals, such robrrt rats Pedersen and Blass, ; Smotherman, ; Smotherman and Robinson, ; Hepper, ; Molina et al.
In these species, the introduction of odorants into the amnion either by direct infusion or maternal ingestion affects later infantile responses to the same stimuli. These studies in non-primate species highlight robeet fact that chemosensory information is part of the normal experience of the foetus. It is the aim of the present study to examine whether similar prenatal facilitative or inductive processes [in the sense of Gottlieb Gottlieb, ] might operate in the formation of the earliest selective responses to odours in human infants.
Taking advantage of the widespread use of anise flavour in the local Alsatian cuisine and of the fact that it is readily perceived by newborns immediately after birth Stirnimann, ; Engen and Lipsitt,we studied odour-elicited responses in infants born to mothers kuhel had regularly consumed anise flavoured sweets or drinks during late pregnancy and infants born to mothers who had not ingested such products during pregnancy.
In the last two gestational weeks i. Miller, Strasbourg, France and sirup Teisseire, Grenoble, France which they could ingest ad libitumbut without changing their customary intake rate.
During this period, they were also asked to fill out a detailed record of their eating habits and of their actual consumption of anise flavoured foodstuffs. By decoding these records and using the quantitative informations provided by dixeo fabricants on the flavour content of the kiehl foodstuffs, we could precisely evaluate the amount of dieo flavour consumed by each individual mother.
The AC group consumed anise flavour on an average of 5. Over the same dise, the group of nAC mothers ingested no food in which anethole constituted the dominant flavour.
AC mothers ceased to consume anise flavour before the onset of labour average time between last anise intake and delivery The newborns were tested with anethole, the pure anise flavour Guenther, most abundantly used in the above sweets or sirup as indicated by the respective companies. The anethole was diluted to a subjective intensity corresponding to that of amniotic fluid. The final dilution step of anethole in paraffin dobert, which represented the best match in subjective intensity with amniotic fluid, was 1.
The solvent, paraffin oil, was used as the control stimulus. Both groups of infants were compared along several behavioural measures of immediate responsiveness: To assess whether the arousing property of the prenatally experienced odorant has a longer lasting effect during early development, the infants were examined within the first 8 postnatal hours mean age 2. The day-of-birth test was run before the infants had had their first postnatal ingestive experience. The day 4 test was run while the infants were in a preprandial state [mean duration since last feed in AC infants 3.
Two tests were conducted on days 1 and 4. In the first test, the infants were sitting immobile in a reclining chair to be videotaped for odour-elicited oral and facial movements. The cotton swabs were mounted on 20 cm long sticks in order to avoid possible contamination with hand odours. In the second test a two-choice paradigm was used.
The subjects sat in a semi-reclining seat facing a standardized visual scene in a dim light environment. Head orientation responses were recorded during two 1 min trials between which the lateral position of the stimuli was reversed. The duration of orientation to each of the stimuli was eiseo across both trials of each test. In addition to the within-subject alternation disel side of stimulus presentation, the relative position of the two stimuli was also systematically alternated between subjects.
On the day 4 follow-up testing, each group comprised 10 subjects the sample reduction was due to two mothers leaving earlier than day ce and to two infants contracting neonatal jaundice. The responses were coded during the stimulus presentation period 10 s and during an additional post-stimulus period 10 s. We used an anatomically based coding scheme of minimally distinguishable motions of the facial muscles [Facial Action Coding System, adult version Ekman and Friesen, and infant version H.
Rosenstein, unpublished manuscript ]. In the light of previous studies which found that negative facial configurations were more discriminant than positive configurations in gauging odour-elicited hedonic responsiveness in newborns Steiner, ; Soussignan et al.
Specifically, all facial configurations, including action units 4 brow lowering9 nose wrinkling10 upper lip raising15 lip corner depressing20 lip stretching26 and 27 gaping and 51 and 52 head turningwere systematically decoded and timed Figure 1. The video records of the two-odour choice test served to code the duration of head orientation to either stimulus.
Diseno de Experimentos – 2b* Edicion : Robert O Kuehl :
Twelve and 10 infants from each group were subjected to these tests on the day of birth and day 4, respectively the reduction in group size being the same as above. The total time oriented to each stimulus was obtained by adding the different orientation durations recorded across the two consecutive trials composing each test. The duration of orientation towards a given stimulus is reported as the mean proportion of time spent oriented towards that stimulus sector as a function of the total time of orientation to the two stimulus sectors and the two stimulus-free sectors.
To assess the differential effects of the odour stimuli on responsiveness in the oro-facial tests the frequencies of infants responding to either stimulus were compared using the Fisher exact probability test for contrasts between the AC and nAC groups and binomial tests were used for within-group comparisons of frequency of responding to the anise versus control stimuli. Treatment and stimulus effects on the duration of facial and mouthing actions in the oro-facial tests and on the relative duration of head orientation in the two-odour choice tests were analysed using two-way repeated analyses of variance ANOVAs on the data of the day-of-birth tests.
Two independent factors were considered as potential determinants of differential responding of the infants, namely stimulus quality anise odour versus control odour and the exposure group AC versus nAC. To assess main or interaction effects due to age, testing time day of birth versus day 4 was entered as an additional factor in the ANOVA design for the data from the infants that could be followed up to day 4. Fisher exact probability tests were also used to compare the number of infants who spent longer oriented to stimulus A than to stimulus B and the number of infants who exhibited the reverse pattern in the two-choice odour tests.
Thus, depending on whether or not their mothers ingested anise flavoured sweets or drinks during the last days of pregnancy, the infants in this study displayed differential facial and oral responses to a pure anise odour within the first hour following birth.
Further evidence for the effect of prenatal exposure to anise on early postnatal responding to anise odour was provided by the head orientation test.
While the AC newborns oriented their head to the anise odour longer than to the control stimulus, the nAC infants did not show a differential duration of head orientation [matched sample t -tests: Thus, at 3 h of age, the newborn infants of this study used previously gained odour information to make decisions supporting directional head motions.
Because the local infant care routine ensured that newborns were minimally exposed to amniotic fluid odour after birth i. To assess whether such prenatal odour priming can influence behaviour for a period longer than the first postnatal hour, the infants of both groups were administered the same oro-facial and two-choice tests on day 4. This suggests that prenatal plus potential postnatal exposure to anise does not have a stronger effect than prenatal exposure alone on the expression of preference for anise on day 4.
On day 4, the frequency of infants displaying negative facial actions and mouthing in response to the odour of anise, as well as the durations of these responses, were no longer affected by whether or not the pregnant mothers consumed anise flavoured foods Figure 3 A,B.
Individual data corroborated this result, i. These data show that behavioural effects attributable to prenatal experience with anise can still be demonstrated 4 days after exposure cessation. Interestingly, the multiple measures of infant response to anise odour appeared to follow different developmental pathways. While the head turning response constituted a stable index of retention of the prenatal odour in the newborns of AC mothers, anise-related oral and facial responses shifted between the first postnatal hour and day 4 in both groups of infants.
Neonatal head orientation is generally held as reflecting the coordinated output of a general mechanism expressing sensation seeking and recognition memory Kuhl,whereas oral and facial responses are seen at this early age as reflecting the stimulus-bound operation of a selective hedonic monitor tied to ingestion Lipsitt, ; Steiner, ; Soussignan et al. This leads to the expectation that oro-facial responses would be more sensitive to the influence of recent ingestive experience and, hence, would show greater plasticity than head orientation.
The present results are consistent with this view. Implicit in the notion that the earliest oral and facial responses are influenced by earlier perceptual learning is that opportunities for such processes actually exist in utero. First, real-time ultrasonographic recordings clearly show that mouthing movements i. Second, the frequent mouthing activity to anise odour observed 3 h after birth in AC infants may be the result of an anise—mouthing contingency established within the days before birth.
Such positive acquisition processes involving the chemical senses may be engaged in the foetus at each episode of ingestion by the pregnant mother in the following way: The exposure of the rapidly developing brain to this cascade of events that recurs at each maternal meal might thus result in the establishment of a functional link between a chemosensory cue and foetal behavioural effectors. Such a functional link may support different behavioural outcomes either by boosting positive responses e.
Following the above logic, infants from nAC mothers could not have attached any positive reinforcing value to the odour of anise and, accordingly, did not display increased appetitive head turning or consumatory mouthing movements in response to it at either age of testing. Nonetheless, at 3 h of age the anise odour evoked more negative facial actions in these infants than in infants born to AC mothers, a pattern of facial response that may be elicited by neophobia.
The disappearance of these anise-linked negative facial motions at 4 days of age in the nAC group may be interpreted in terms of maturation or of attenuation of neophobia due to anise exposure in the previous test session.
This interpretation raises the possibility of very rapid odour familiarization shortly after birth. To our knowledge, this study represents the first evidence that oral and facial correlates of hedonic processing in the newborn infant can be influenced by prenatal chemosensory experience.
Previous suggestive attempts had only noted discriminative Schaal and Orgeur, or reduced aversive Hepper, responses of newborns to an aroma consumed by the pregnant mother. More specifically, within the first 4 days after birth infants not only recognize the individual signature of the amniotic fluid they inhaled during the last days before term Marlier et al. Thus, selective perception and learning of odour information is possible near gestational term. Finally, at the same time as it shapes olfactory perception and cognition, intra-uterine odour experience sets the motivational frame in which the oriented behaviour of the infant initially develops.
Odour learning within the amnion becomes coupled with more or less plastic motor patterns.
Diseno de Experimentos – 2b* Edicion
In the case of head orientation, the prenatally acquired odour—response link persists for at least the first 4 postnatal days. Thus, foetal olfaction fosters the acquisition of predictable sensory information upon which neonates can rely during a period when they encounter a variety of vital micro- and macro-transitions in the context of variable and unprecedented stimuli [e.
It can thus be expected that the acceptance at weaning of non-milk foods is influenced by their congruence with odour qualities resembling those encountered in the weeks or days before birth. Representative examples of facial expressions of awake newborns exposed to 10 s anise odor stimuli.
Infant a belongs to the anise-exposed group; infants b — d belong to the non-anise-exposed group. Mean duration of A negative facial configurations, of B mouthing activities and of C head orientation in response to the presentation of anise odor solid bars and the control stimulus empty bars to infants of an average age of 2. Results in A and B derive from successive presentations of the two stimuli, while results in C derive from simultaneous presentation. Mean duration of A negative facial configurations, of B mouthing activities and of C head orientation in response to the presentation of anise odor solid bars and the control stimulus empty bars to infants aged 4 days of mothers consuming anise AC or not nAC during gestation.
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Barry Keverne, Richard E. Tremblay and Gerald Turkewitz and Ms Denise Urquhart and Elisabeth Hertling for their helpful thoughts and comments on a previous draft. Additional support was obtained from the Benfaro Foundation to R. Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide.
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