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For Peer Review Human awareness and uses of odor cues in everyday life: Results from a questionnaire study in children Journal: International Journal of Behavioral Development Manuscript ID: IJBD-2006-08-0655.R2 Manuscript Type: Original Manuscript Keywords: elementary school children, perception, individual differences, gender differences, ecological context Abstract: The Children's Olfactory Behavior in Everyday Life questionnaire was developed to assess attention to, and uses of, odors in real life situations, and to evaluate individual variations. The tool comprises 16 items prompting self reports of active seeking, awareness and affective reactivity to odors of food, people and environment. Children (102 girls, 113 boys), aged 6 to 10 years, participated in the study. The results revealed that girls were significantly more olfaction-oriented than boys, especially towards odors of people, self, and the environment. An increasing ability of children to describe the odor facets of their perceptual world was found between 6 and 10, partly due to ameliorating verbal skills. Finally, owning an 'attachment object' was linked to olfactory reactivity to odors, especially in social and affective contexts. Overall, this research contributes to expand our understanding of the behavioral importance of odors in children and its individual variations, and it brings additional arguments against the prevalent concept of functional microsmaty applied to the human species. http://mc.manuscriptcentral.com/ijbd International Journal of Behavioral Development

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For Peer ReviewHuman awareness and uses of odor cues in everyday life: Results from a

questionnaire study in children

Journal: International Journal of Behavioral Development

Manuscript ID: IJBD-2006-08-0655.R2

Manuscript Type: Original Manuscript

Keywords:elementary school children, perception, individual differences, gender differences, ecological context

Abstract:

The Children's Olfactory Behavior in Everyday Life questionnaire was developed to assess attention to, and uses of, odors in real life situations, and to evaluate individual variations. The tool comprises 16 items prompting self reports of active seeking, awareness and affective reactivity to odors of food, people and environment. Children (102 girls, 113 boys), aged 6 to 10 years, participated in the study. The results revealed that girls were significantly more olfaction-oriented than boys, especially towards odors of people, self, and the environment. An increasing ability of children to describe the odor facets of their perceptual world was found between 6 and 10, partly due to ameliorating verbal skills. Finally, owning an 'attachment object' was linked to olfactory reactivity to odors, especially in social and affective contexts. Overall, this research contributes to expand our understanding of the behavioral importance of odors in children and its individual variations, and it brings additional arguments against the prevalent concept of functional microsmaty applied to the human species.

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INTRODUCTION

Despite considerable advances in understanding molecular and neural mechanisms of

olfaction (e.g., Doty, 2003; Finger, Silver & Restrepo, 2000), its functions in the everyday life

of humans remain little understood. For some scholars, the adaptive significance of the sense

of smell in our own species has undergone an anatomical decline with the evolutionary

sophistication of visual perception and cognition (Gilad, Wiebe, Przeworski, Lancet & Pääbo,

2004; Rouquier, Blancher & Giorgi, 2000). The human species is thus considered as

"microsmatic", i.e. having morphologically reduced olfactory structures, and hence poor

olfactory function. However, other sources suggest that olfaction remains highly serviceable

in multiple essential functions (Candau, 2000; Herz, 2002; Schaal & Porter, 1991; Shepherd,

2004). For example, acute perturbations or the chronic loss of smell greatly affect quality of

life (e.g., enjoyment of food, social partners, and the general environment), and jeopardize the

control of potentially unsafe circumstances (e.g., fire, cooking, cleanliness, disease; Hummel

& Nordin, 2005; Tennen, Affleck & Mendola, 1991; Van Toller, 1999). Conversely,

excessive odor levels in the environment can lead to annoyance and related psychological or

social disorders (Lax & Henneberger, 1995; Schiffman, Studwell, Landerman, Berman &

Sundy, 2005). Besides such defective or excessive odor input, humans generally rely –

consciously or not – on olfactory cues to direct selective attitudes and actions (Degel &

Köster, 1998; Hermans & Baeyens, 2002; Spangenberg, Crowley & Henderson, 1996).

Although anthropological records point to universal human reliance on olfaction (Classen,

Howes & Synnott, 1994; Howes, 2002; Schaal, 2004), individuals can differ in the everyday

valuation of the sense of smell. These differences may pertain to psychobiological

propensities controlled by genetic determinants, individual exposure effects, gender,

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development or health variables, or to more general influences linked with cultural biases or

expertise (e.g. Wysocki, Pierce & Gilbert, 1991). Inter-individual variations in olfaction are

already present early in development, in infants and children. While some kids overtly rely on

odors in their feeding or social orientations, some developing even odor-based stereotypes or

phobias (Brill, 1932; Schaal, 1996), others do apparently not care. Such early variations have

barely been quantified, especially in everyday contexts, although parents often report

contrasted olfactory reactivity among their offspring.

Children represent a well-suited target to investigate both general olfactory cognition in daily

settings and the degree of its variability between individuals. First, school-aged children have

good enough mastery of language to report details of their perceptions and affective reactions.

Second, children generally display less inhibition than adults in describing their intimate

feelings, such as those associated with social olfaction. Third, they possess keen olfactory

abilities – sometimes outdoing those of adults (for review, cf. Schaal, 1999) – when tested in

laboratory settings involving odorants presented explicitly: detection thresholds,

discrimination, recognition, identification, description of related impressions and preferences

(Cain et al., 1995; Lehrner, Gluck & Laska, 1999; Richman, Sheehe, Wallace, Hyde &

Coplan, 1995; Schaal, 1988; Schmidt & Beauchamp, 1988). Besides this substantial bunch of

perceptual data, only few studies have investigated children’s actual uses of olfaction in

common life situations. For example, children are able to distinguish odors of significant

others (parents, siblings, friends) and of themselves from those of unfamiliar individuals

(Mallet & Schaal, 1998; Montagner, 1974). In playing children, modeling clays differing by

smell triggered emotional reactions depending on the hedonic valence of the smell (Barnham

& Broughan, 2002). Rodionova and Minor (2005) found that the odorization of classrooms

enhanced or decreased (depending on the odorant used) children’s attentional and executive

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performances in school tasks. Moreover, several studies suggest that odors encountered in

positive or negative emotional contexts can be recorded as cues influencing subsequent

behavior and preferences. Children performed indeed worse in an attention task when the

ambient air was scented with an odor previously encountered in a frustrating context (Epple &

Herz, 1999). Otherwise, their appreciation of the smell of tobacco and alcohol depended on

their parents' emotional states (either positive or negative) associated with the use of these

substances (Mennella & Beauchamp, 1998; Mennella & Garcia, 2000). Finally, own body

odor seems to be sought after by children, e.g. through the use of so-called ‘attachment

objects’ (generally a soft toy or a piece of cloth carrying such stimulations), and might have a

positive effect on children’s emotional homeostasis (Schaal, 1988), but this point remains

largely unexplored. Altogether, these data indicate that, in real-life situations, odors can

interfere with affective states and cognitive performances in children. However, the everyday

impact of odors remains scarcely understood in children, and it is the aim of the present study

to better appreciate the phenomenology of children’s awareness of ecological odors and to

characterize individual differences in their reliance on smell.

As a first approach, we opted for the questionnaire method. Previous investigators already

employed this way to address the impact of olfactory stimuli on feelings, attitudes and

behaviors in adults (Cupchik, Phillips & Truong, 2005; Herz & Inzlicht, 2002; Martin, Apena,

Chaudry, Mulligan & Nixon, 2001; Nordin, Millqvist, Löwhagen & Bende, 2003;

Wrzesniewski, McCauley & Rozin, 1999). To our knowledge, only one similar instrument

was designed for children, the so-called Sensory Profile (Dunn, 1994, 1997; completed by

adults). As this questionnaire included only 5 odor-related items embedded in 125 items and

focused on sensori-motor defects, it appeared not suited to investigate olfaction in non-

clinical samples. Based on the fruitful application of questionnaires in adults and on their lack

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in children, we developed a tool to probe Children’s Olfactory Behavior in Everyday Life

(COBEL) in a pilot study. According to the limited attentional, mnesic and verbal skills of the

participants, the priority was given to reduce task complexity and length, and to stimulate the

children’s attention and motivation (familiar vocabulary, limited number of items, variable

response modes). The aim of the COBEL questionnaire was to prompt children’s responses to

situations involving food, social and other environmental odors, and to trace different types of

behaviors, such as active seeking of odors (intentional inhalation of odors), awareness of

odors (ability to notice, memorize and name odors) and affective responses (hedonic

reactivity, idiosyncratic valuation of given odorous objects).

After presenting some reliability aspects of the developed tool, we first analyze the content of

school-aged participants’ answers to the COBEL, which brings new insights on the children’s

daily olfactory behaviors. The second main point of the present study is to focus on inter-

individual variations, especially as a function of gender and age. As females are known to

display better olfactory skills than males with artificial and real-life odorants (adults: Dalton,

Doolittle & Breslin, 2002; Koelega & Köster, 1974; Le Magnen, 1952; children: Doty et al.,

1984; Moncrieff, 1966; Richman, Wallace & Sheehe, 1995), we hypothesized that girls would

report higher attention and reactivity to odors, i.e. would have higher COBEL scores. Several

olfactory skills, such as odor memory and odor identification, have been shown to increase

during childhood (Jehl & Murphy, 1998; Richman et al., 1995b). Therefore, we expected the

COBEL scores to increase during school years as a result of both experience and cognitive

development. Finally, we make a special case of children’s reactions to the odor of their

attachment object. Winnicott (1958) widely described this object as having a transitional

function during the separation between mother and child. This familiar object is known to act

as a comforter and a soother, allowing the child to face stressful situations. The distinctive

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odor of attachment objects has recurrently been pointed out (Mahalski, 1983; Schaal, 1988;

Winnicott, 1958), but its contribution to the comforting value of the object has never been

investigated in depth. Thus, if smell is a salient attribute of attachment objects, children

should describe marked olfactory behaviors with them and owning such objects should be

somewhat linked to the general reliance on olfaction.

METHOD

Participants

Children (N = 215) were recruited in three elementary schools of Dijon. Five age groups were

constituted: 6- (girls/boys: 19/20), 7- (24/31), 8- (25/26), 9- (25/22) and 10-year-olds (9/14).

Some participants were siblings (2 triplets of boys including one pair of twins, 5 pairs of girls

including one of twins, 4 pairs of boys including one of twins, and 9 girl-boy pairs). These

siblings were all included as their responses to the questionnaire did not converge (Pearson

correlation of total COBEL score by pairs: r(23) = .10, p = .659). The ethnical background

determined by the experimenter was approximately 90% Europe and 10% Africa.

Authorizations to conduct this study in the schools were obtained from the local School Board

and school directors. Informed written consent from parents was required before entering a

child in the study, and the anonymity of the participants’ answers was preserved.

Instruments and tasks

COBEL questionnaire

The participants gave self-reports of their olfactory behaviors following the COBEL grid. The

questions were related to attitudes and behaviors (active seeking, awareness, and affective

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reactions) triggered by food, social, or more general environmental contexts involving

olfaction. The questionnaire is presented here in English, although it was passed in French (cf.

Appendix). The order in which the items were given (item numbers) was set so that items not

mentioning odors were given first to probe spontaneous odor-related responses. Besides, all

items were grouped by context (food, environment, social) to limit the participants’ feeling of

scrambled questions, and items related to intimate or body issues were placed at the end of the

questionnaire, when the participants were presumed to feel more comfortable with the

interviewer. Finally, to spur continued incentive during the interview, mixed answering

modes were prompted, using structured (multiple-choice answers, 3-point rating scales, yes-

no and classificatory answers, i.e., importance of smell compared to other senses in given

situations) and unstructured modes (open-ended answers). To score each item (cf. Appendix),

a 3-point scale was used to rate the behavior as poorly (0), moderately (0.5) or highly (1)

olfaction-oriented in the aimed situation. The scores of the 16 items were summed, resulting

in a total COBEL score ranging from 0 to 16. Finally, to analyze the children’s raw answers

to open questions, categories were constituted a posteriori.

Two additional questions asked at the beginning of the interview enquired about the use of

attachment objects (AOs). As not all participants prized such objects, these questions were not

included in the computation of the total COBEL score.

Verbal fluency assessment

To control for individual differences in general verbal abilities, the children performed a

verbal fluency task in which they had to utter as many fruit names as possible in 60 sec and

then words beginning with the letter ‘b’ during the same time (Benton & Hamsher, 1976;

Hurks et al., 2006; Sauzéon, Lestage, Raboutet, N’Kaoua & Claverie, 2004). The number of

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correct ‘fruit’ and ‘b’ words were summed and transformed into z-scores to form a verbal

fluency score. Moreover, the sample was split in two groups composed by fluent (z-score ≥ 0)

and less fluent (z-score < 0) children.

Procedure

Two female interviewers noted the answers of the children to the 16 items of the COBEL and

to the verbal fluency test. Each session lasted for about 20 min per child. The participants

were interviewed individually in a quiet schoolroom. The participants, unaware that they shall

be questioned about odors, were instructed as follows: “I will ask you some questions about

your everyday life. It is not like a school test, there is no right or wrong answer. Just tell what

you feel, what you think and what you usually do. What you will say will remain between us,

so do not feel embarrassed. Do not hesitate to tell me if you do not understand something.”

At the end of the session, the participants were required not to tell their classmates the topic of

the questionnaire. To verify that the children did not influence each other, every classroom

was split into two halves according to the timing of the interviews. A t-test ascertained that

the scores of the children passing last were not higher than those of the children passing first

(Mean±SD = 6.4±2.4 vs. 7.0±2.4, respectively; t(213) = 1.62, p = .106).

The verbal fluency task was presented as a game during which children had to name aloud “as

many words as possible in one minute”. Before beginning the task itself, the experimenter

gave examples with the ‘animal’ category and the letter ‘m’.

Statistical analyses

The psychometric properties of the COBEL questionnaire were determined by means of inter-

item gamma correlations (Goodman & Kruskal, 1954; Siegel & Castellan, 1988) and alpha

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coefficient (Kline, 1993) computed from the gamma correlation matrix. We evaluated the

effects of gender [N(girls, boys) = 102, 113] and age [N(6, 7, 8, 9, 10 year-olds) = 39, 55, 51,

47, 23] on the total COBEL score with analyses of variance (ANOVA) and on the separate

item scores with non parametric methods: Mann-Whitney U-tests for age and Kruskal-Wallis

analyses of variance for gender effects. Chi-square tests were used to test gender and age

effects on the contents of raw answers. Finally, the impact of verbal fluency [N(fluent, less

fluent) = 106, 109] on the total and item scores was quantified respectively through a

covariance analysis (ANCOVA) and through Mann-Whitney U-tests. The links between the

variables related to the attachment object and the COBEL scores were analyzed by means of

t-tests (total score) and Mann-Whitney U-tests (separate item scores). Data are given as mean

values ± standard deviation and statistical significance is set at p < .05.

RESULTS

Psychometric properties

The average total COBEL score of the sample was 6.7±2.4 and followed a normal distribution

(Kolmogorov-Smirnov test: d = .082, ns). The range of values was ample (1.5-13.5), nearly

filling out the scale (0-16) without bottom or ceiling effects. Inter-item gamma correlations

were comprised between -.22 and +.66 (.19 on average), confirming that the items were not

redundant. The alpha coefficient computed from the gamma correlation matrix was .78,

suggesting a good internal consistency of the questionnaire.

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Children’s olfactory ecology

The detailed analyses of the children’s raw answers are presented in Table 1. The answers to

the food items highlight the importance of the chemosensory dimension of food, since these

sensory properties motivated the rejection of two thirds of the disliked foods and since a

majority of children reported sampling the smell of unknown foods and guessing food odors.

Some children (a 7-year-old boy and a 6-year-old girl) spontaneously dissociated the smell of

food and their appreciation of it, insisting on the point that a food with a bad smell (e.g.,

cheese) might nevertheless taste good.

Insert Table 1 about here

Concerning social odors, a majority of children were aware of people’s odor, especially that

of relatives, to which they reported to be particularly attached (Table 1). High percentages of

participants also reported to sample self odor (from the body or the clothes). Even for items

not specifically directed to social situations, the odor of people and self came out

spontaneously, indicating their salience (items 4-Yesterday odors, 5-Odors sought when sad,

and 6-Treasured odorous objects, related to affect and memory). In these items, the

designated social odors were mainly those of their attachment object and of relatives.

Finally, children reported to be less oriented towards other smells of the environment

(Table 1), such as odors of bathroom objects and school tools (although some of them are

scented, cited by 7% of the participants). Nevertheless, the children described their marked

affective reactions to odors in cars (rather appreciated) and to the odors of tobacco smoke

(generally depreciated, but not only on sensory grounds). A high percentage of participants

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reported to be fond of smells in the outdoor environment. However, when they had to

compare olfaction with other senses (item 3-Senses in nature), it appeared not to be the most

relevant source of information, at least in this context.

Inter-individual differences

Total COBEL score

A 2 (gender) x 5 (age groups) between-subject design ANOVA yielded significant main

effects of gender (F(1,205) = 24.44, p < .001) and age (F(4,205) = 2.94, p < .05) on the total

COBEL score, but no interaction. The total COBEL score was higher in girls than in boys

(7.5±2.3 vs. 6.0±2.2) and increased with age (from 6.0±2.8 at 6 to 7.6±2.3 at 10; Fig. 1).

Insert Figure 1 about here

For the verbal fluency z-scores, another age by gender ANOVA showed that girls produced

significantly more words than boys (0.11±1.07 vs. -0.10±0.93; F(1,205) = 4.13, p < .05).

Expectedly, verbal fluency increased steadily with age (F(4,205) = 19.75, p < .001), without

interaction with gender. Therefore, to test whether age and gender main effects on the total

COBEL score might be due to differences in verbal abilities, an age by gender analysis of

covariance was run with verbal fluency as a covariate. Verbal fluency modulated the COBEL

score (F(1,204) = 5.50, p < .05), but whereas the significant main effect of age on the total

COBEL score vanished when fluency was entered as a covariate (F(4,204) = 1.44, p = .221),

the main effect of gender remained highly significant (F(1,204) = 21.33, p < .001). Thus, the

higher female COBEL score appeared not to be the mere outcome of female verbal advantage.

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Separate items

The detailed analyses of the effects of gender, age, and verbal fluency are presented in

Table 2. Overall, the answers of girls indicated that their behaviors are clearly more olfaction-

oriented than those of boys. The superiority of girls in reporting attention and reactivity to

odors was statistically ascertained for 8 out of 16 item scores, involving social (items 11, 13

and 14) and environmental odors (items 3, 5, 6, 9 and 10), but not food. They reported to

attach more importance to smell when asked to compare several senses (item 3-Senses in

nature). Detailed analyses of the raw answers revealed additional gender effects (items 7 and

15) that did not appear in the analysis of the item scores. A higher proportion of girls in

item 7-Outside odors reported they would be annoyed in the absence of odors outside home

(80% of the girls vs. 67% of the boys, χ2 = 4.75, p < .05). In item 15-Tobacco smell, girls

reported less frequently indifference to the smell of tobacco smoke (1% of the girls vs. 11%

of the boys, χ2 = 8.77, p < .01) and more often aversive reactions (97% of the girls vs. 82% of

the boys, χ2 = 12.22, p < .001). Overall, two thirds of the items are thus affected by gender

effects, always in favor of girls.

Insert Table 2 about here

Otherwise, the scores of five items significantly increased with age (items 1, 4, 10, 12 and 16;

Table 2). Additionally to the increasing score of item 1-Odor in food dislikes, we noticed that

the number of different justifications used to explain food dislikes increased with age (from

1.5±0.9 at 6 to 2.4±1.3 at 10, F(4,205) = 3.15, p < .05). As for gender effects, detailed

analyses of the raw answers revealed additional age effects in two items (5 and 11). For item

5-Odors sought when sad, an age-increasing number of children cited objects carrying social

odors as objects especially sought when they feel sad (χ2 = 12.99, p < .05) and a decreasing

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number of children relied on food-related odors in the same context (χ2 = 10.53, p < .05). For

item 11-Family odors, the proportion of participants being aware of the odor of their relatives

increased from 62% at 6 years to 96% at 10 (χ2 = 10.70, p < .05). Moreover, to explain why

they would be annoyed to lose their relatives’ odor, children mentioned decreasingly between

6 and 10 years the loss of a pleasant stimulus and increasingly the loss of a reassuring cue

(χ2 = 10.06 and 12.04 respectively, p < .05 in both cases).

Finally, verbal fluency (which ameliorated with age and was higher in girls) was found to

have a limited influence on the item scores, affecting the outcome of only three items (items

3, 4 and 12; Table 2). Children with higher verbal fluency had higher scores on item 4-

Yesterday odors and 12-People’s natural odor. These results suggest that language and

cognitive abilities may underlie the increase of these item scores with age. However, the fact

that children with lower fluency had higher scores on item 3-Senses in nature does not allow

to explain the girls’ higher score to this item.

Attachment objects and olfaction

The detailed analyses of the answers concerning the AO are given in Table 1. Most children

reported having or having had an AO, and a notable proportion of them spontaneously

reported olfactory behaviors towards this object. While some children declared they liked

their AO to be washed [e.g., “It smells better” (girl, 8 years)], several reported a preference

for the AO’s ‘natural’ odor [“It does not smell like me anymore” (girl, 8), “I like its odor

when it stinks” (girl, 7)]. Oro-nasal contacts, concerning dolls and cloths more than cuddly

toys (χ2 = 17.64, p < .001), were also reported [“I put the ears of my hippo inside my nose”

(boy, 8), “I take a thread from my towel and rub it round my mouth” (girl, 9), “I sniff at one

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of my rabbit’s ears while I suck my thumb” (boy, 6)]. No gender differences came out for

these variables. However, the proportion of participants currently being fond of an AO

decreased with age (from 82% of the 6-year-olds to 52% of the 10-year-olds; χ2 = 20.56,

p < .001). Moreover, the proportion of participants reacting to the change of the AO’s odor

after washing increased between 6 and 10 years (from 13% to 57%; χ2 = 14.46, p < .01).

Insert Table 3 about here

The significant links between the variables related to the AO and the total COBEL score, as

well as scores on individual items, are presented in Table 3. It comes out that reported

olfactory behaviors towards the AO were linked to the general olfactory awareness (total

COBEL score) and to specific olfactory behaviors involving social odors (either directly: item

12-People’s natural odor; or indirectly: items 4-Yesterday odors and 5-Odors sought when

sad). These links were particularly significant with item 5. This item refers to consolation

situations, when AOs are also often manipulated and olfactorily exploited (15% of the

participants reported seeking the odor of their AO in such situations, cf. Table 1).

Interestingly, the mere possession of an AO was related to the reported propensity to smell

own body. Finally, two items focusing on the wider environment (3-Senses in nature and 7-

Outside odors) were also linked with AO variables.

DISCUSSION

Questioning children about their everyday olfactory experience

The present study aimed to assess children’s olfactory behavior in everyday life settings. The

COBEL questionnaire appeared to have acceptable psychometric properties (item

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discriminating power and internal consistency). Although olfactory perception is reputed to be

poorly verbalized in adults as well as in youngsters (Cain, 1977; Engen, 1987; Engen &

Engen, 1997), the COBEL questionnaire succeeded in providing a detailed and substantial set

of information about children’s olfactory Merkwelt (von Uexküll, 1909). In our 6-to-10 year-

old sample, the prevalence of olfactory behaviors was high for most items, suggesting that

odors are significant cues for children in the targeted situations. The implication of social

odors from others and self in the children’s affective life were spontaneously and recurrently

mentioned. We also noted that olfaction was considered of minor relative importance when

ordered among other senses (item 3-Senses in nature). This result corresponds to the popular

belief that vision dominates human perception. However, when people are interviewed about

the importance of the five senses in evaluating various consumer goods, this popular belief

can easily be dismissed for some products (Schifferstein, 2006). In the present study, odors

are not considered as very salient sources of children’s experience during outdoor walking,

but their importance is revealed in other contexts, specifically those involving interpersonal

relations.

Individual differences in reported olfactory behaviors

The use of the COBEL in a large non-clinical sample of 6-to-10 year-olds revealed that girls

reported significantly higher attention and reactivity to odors in daily settings. This result

appeared not to be conditional upon gender differences in verbal/semantic skills. The gender

differences revealed by the COBEL are in agreement with adult questionnaire studies (Herz &

Inzlicht, 2002; Martin et al., 2001; Nordin, Bende & Millqvist, 2004) and indicate that the

stronger odor-orientation of human females is established from an early age onwards.

Specifically, girls reported higher attention and reactivity to social odors of others and self, to

some environmental odors (home and outdoor, car, tobacco smoke) and to affect-laden odors

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(items 5-Odors sought when sad and 6-Treasured odorous objects), but not to food odors.

Altogether, these results concur with current data on gender differences in affective reactivity

to odors (Doty, 1986; Olofsson & Nordin, 2004), olfactory cognition (Cain, 1982; Doty et al.,

1984; Richman et al., 1995b) and sensitivity (Dalton et al., 2002; Kobal et al., 2001; Koelega

& Köster, 1974). To understand why growing up as a female or a male leads to early different

chemo-perceptual and cognitive outcomes, it seems necessary to untie these ‘package’

variables which are not explanatory per se, but rather represent a collection of

psychobiological and socio-cultural determinants (Gauvain, 1995). Children learn to solve

everyday issues in their developmental niche (Super & Harkness, 1986), i.e. their normative

contexts of events, practices, representations, and values. In western urban cultures, females

are indisputably and ubiquitously more frequently than males exposed to odors in specific

functional contexts, such as cosmetic use, child care (Geary, 1998) and housework (Eurostat,

2004; Fuwa & Cohen, 2006). They certainly are (taught to be) more concerned with the

control of environmental and body odors (Mallet & Schaal, 1998; Wysocki et al., 1991),

which probably explains their deeper olfactory expertise in recognizing body odors and in

relying on odors in self-assessment and sexual interaction (Herz & Inzlicht, 2002; Platek,

Burch & Gallup, 2001; Schleidt, Hold & Attili, 1981). Olfactory experience may be

differentiated early in girls through the early affordance of odorized objects (e.g., scented

toys, school tools and accessories) and modeling of mother’s activities. In that context, young

females may be more than boys under social pressure providing both opportunities for, and

constraints on, the valuation of odors as significant cues. As a consequence, girls are already

more concerned with the odor of significant others from age 4-6 years (Mallet & Schaal,

1998; Verron & Gaultier, 1976) and with a wide variety of odors (the present study). In

addition, such early gender differences in awareness and reactivity to social odors may derive

both from greater promiscuity in the prosocial behavior of females (Eagly, 1987; Haviland &

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Malatesta, 1981) and from a general tendency of females to react more intensely to emotional

stimuli (Geary, 1998; Sharp, van Goozen & Goodyer, 2006), among which odors are not the

least (Engen, 1982; Herz, 2004).

The total COBEL score and the score of several separate items were found to ameliorate over

the 6-10 year period, a result well aligned with previous findings on the development of

olfactory sensitivity, discrimination, memory and identification (Cain et al., 1995; Doty et al.,

1984; Hvastja & Zanuttini, 1989; Koelega, 1994; Richman et al., 1995a,b). Children show

indeed age-enhanced knowledge on the odors of people, objects and food, and higher ability

to recall odors. Moreover, their understanding of internal states related to odors becomes

better, as shown by their improved and more complex descriptions. As in a study by Oram et

al. (1995), they become more analytic in extracting odors from multimodal stimuli. These age

effects may derive from the interplay of an expanding exposure to odors and cognitive

maturation. Enhanced memory and lexical abilities (verbal fluency) clearly account for the

increase of the COBEL score with age, as they account for variations in the cognitive

processing of odors in adults (Larsson, Lovden & Nilsson, 2003). Overall, our results show

that 6-10 year-olds show an expanding ability to scrutinize the hidden facets of their sensory

environment and to put such implicit percepts into words. Affective reactions to odors,

however, seem already well established by 6 years, since the more emotionally-colored items

(5, 6, 11, 14, and 15) went unaffected by age.

Olfactory behaviors displayed through attachment objects

The saliency of the olfactory dimension of the AO was spontaneously attested by 27% of the

total sample, and 15% reported active seeking of its distinctive odor as a way to soothe from

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stressful events. An additional argument in favor of the olfactory meaning of these objects is

the link between owning an AO and the higher attention to self body odor (which also

impregnates the AO). Moreover, olfactory behaviors towards the AO and towards odors in

social and affective contexts are related. Overall, these results agree with the commonly-held

hypothesis that self-odor left on the AO may have short-term soothing/reassuring effects on

children. In the longer term, the interaction with an AO might have consequences on the

development of sensory knowledge since it is linked to environmental items of the COBEL.

The mechanisms by which odor experience connected with the AO bridges to olfactory

experience in the wider environment are worthy of future empirical exploration.

Conclusion

The questionnaire on Children’s Olfactory Behavior in Everyday Life is a new method,

inspired by adult studies, to investigate psychological and behavioral aspects of olfactory

function in children. In the future, this tool should be used in complement with laboratory

approaches on olfactory sensitivity, emotional reactivity, and cognition. It contributes both to

expand our knowledge on the daily uses of olfactory cues and to highlight the variability of

olfactory behaviors from childhood onwards. Although the COBEL questionnaire probably

still underestimates the extent to which odors really affect children’s lives, the participants’

reports suggest that olfaction has a significant implication in the regulation of social relations,

food and environmental enjoyment, emotional self-regulation and body care. Moreover, the

importance of odors in daily settings appeared higher in girls than in boys, a topic that would

be worth investigating for its socio-cultural causes and consequences. Overall, this research

points out that olfaction is ubiquitously significant to 6-to-10 year-old children. It brings thus

additional arguments against the common belief that human beings are "microsmatic", a

concept which omits to consider the actual use of olfaction in real life situations.

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Acknowledgements

We gratefully acknowledge the teachers of the Dijon school board and the parents and

children for welcoming our research, C. Marinot and S. Martin for their assistance in data

collection, and Drs C. Granier-Deferre, D. Valentin, and H. Abdi for discussion. Ms N.

Mutin, V. Bué and S. Gros are thanked for logistic and documentary assistance. This study

was supported by CNRS and a doctoral grant from French Ministry of Research (to CF).

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Appendix

Content and scoring method of the 16 items of the COBEL questionnaire and additional items

about the attachment objects.

Food-related olfactory contexts

Item 1 - Odor in food dislikesAre there some foods/drinks that you hate (yes/no)? Which ones (up to 6)? For which reasons (for each cited food)? Scoring: > 2/3 of the reported food items are disliked because of the flavor/odor (1), between 1/3 and 2/3 (0.5), < 1/3 (0).

Item 2 - Response to unknown foodImagine your parents present you a dish you do not know: will you do something before putting it in your mouth (yes/no)? What do you do? Will you smell it (yes/no)? Scoring: the child reports spontaneously smelling the unknown food (1), not spontaneously (0.5), reports not smelling the food (0).

Item 16 - Guessing food odorWhen you smell a food odor, do you try to guess for fun what it is (never/sometimes/ often)? Scoring: often (1), sometimes (0.5), never (0).

Social-related olfactory contexts

Item 11 - Family odorsDo you find that your parents/siblings smell of something? Imagine they would not smell anything anymore: would you not care/would it bother you/would it suit you - a little/a lot? Why? Scoring: bothers or suits the child a lot (1), a little (0.5), the child does not care about it or finds that parents smell nothing (0).

Item 12 - People’s natural odorDo you find that people smell of something, even without perfume or deodorant (no/yes some people/yes everyone)? Scoring: everyone (1), some people (0.5), no (0).

Item 13 - Smelling clothesDo you happen to smell your clothes (never/sometimes/often)? Why? Scoring: often (1), sometimes (0.5), never (0).

Item 14 - Smelling self-odorDo you happen to smell parts of your body (never/sometimes/often)? Which parts? Why?Scoring: often (1), sometimes (0.5), never (0).

Environment-related olfactory contexts

Item 3 - Senses in natureWhen you walk in nature, what do you prefer (rank from 1 to 4: touching, smelling, watching, listening)? Scoring: smelling is placed 1st or 2nd (1), 3rd (0.5), 4th (0).

Item 4 - Yesterday odorsDo you remember odors you smelled yesterday (food odors not acceptable)? Which ones? Scoring: several odors are cited (1), one odor is cited (0.5), the child does not remember (0).

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Item 5 - Odors sought when sad Are there odors you like smelling when you feel sad? Which ones? Scoring: several odors are cited (1), one odor is cited (0.5), no odor is cited (0).

Item 6 - Treasured odorous objectsAre there things you treasure just because they smell very good? Scoring: several objects are cited (1), one object is cited (0.5), no object is cited (0).

Item 7 - Outside odorsImagine there would be no odors anymore outside: would you not care/would it bother you/would it suit you - a little/a lot? Scoring: it annoys or suits the child a lot (1), a little (0.5), the child does not care about it (0).

Item 8 - Smelling school toolsDo you happen to smell your school things (never/sometimes/often)? Which ones? Scoring: often (1), sometimes (0.5), never (0).

Item 9 - Odor in carsIn your parents’ car, does it smell something or nothing? Do you love/like/not care/not like this odor /feel ill? Scoring: the child loves the car’s odor or feels ill (1), likes or does not like it (0.5), does not care about it (0).

Item 10 - Odor of bathroom objectsPlease list objects of your bathroom (up to 8). Which ones smell of something? Scoring: > 2/3 of the objects are odorous (1), between 1/3 and 2/3 (0.5), < 1/3 (0).

Item 15 - Tobacco smellImagine someone is smoking next to you. Do you love/like/not care/not like/hate this odor? Scoring: the child loves or hates the odor (1), likes or does not like it (0.5), does not care about it (0).

Additional items about attachment objects

- Do you have (had) a blanky/soft toy? Do (did) you like, do (did) you dislike, do (did) you not care when your parents wash (washed) it? Why? [asked before item 1]

- When you hold your blanky/soft toy in your hand, what do (did) you like to do with it? [asked between items 3 and 4]

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Figure legend

Fig. 1. Mean COBEL score (± SEM) as a function of gender and age (ANOVA: p < .001 and

p < .05 respectively, N = 215).

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Figure 1

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Age groups (years)

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Table 1. Detailed free and forced-choice raw answers to the COBEL items related to food, social and environmental odors, and to the attachment object AO. Percentages are based on the whole sample (N = 215), except when N is specified. * indicate that multiple answers were allowed, explaining why the sum of percentages is higher than expected.

FOOD 1-Odor in food dislikes67% of the disliked foods are rejected partly because of their smell/flavor (N = 703 cited foods)43% of the reasons to dislike are smell/flavor (57% other: texture, irritation, bitter/sour, visual aspect)(N = 424 cited reasons)

2-Response to unknown food61% of the children smell the unknown food (25% report it spontaneously, 36% only when explicitly asked)

16-Guessing food odor72% try to guess the origin of a food odor (24% often, 48% sometimes)

SOCIAL 11-Family odors77% are aware of their relatives’ odor

� 45% would be bothered to lose their relatives’ odor, it would suit 7% and 25% would not care

� Bothered because of: 22% the loss of a pleasant stimulus, 11% the loss of a reassuring cue, 12% other

12-People’s natural odor53% are aware of the people’s natural odor (16% everybody, 37% only some people)

13-Smelling clothes69% smell their clothes (20% often, 49% sometimes)� 21% smell their clothes to determine cleanliness and 14% good/bad smell, 14% to enjoy,

11% to stimulate/reassure oneself, 14% other *14-Smelling self-odor

52% smell parts of their body (14% often, 38% sometimes)

� 20% smell their hands, 15% feet, 14% armpits, 9% arms, 7% hair, 13% other *� 33% to inquire about good/bad odors and 12% about cleanliness, 8% to stimulate/inform oneself, 9% other *

ENVIR 3-Senses in nature13% place smell at rank 1 of importance (46% sight, 25% touch, 16% hearing), 22% at rank 2, 65% at ranks 3/4

4-Yesterday odors44% recollect odors from the day before (13% at least two, 31% one)

� 12% social odors, 11% nature, 11% cosmetic, 7% pollution, 5% excrement/decomposition, 13% other *

5-Odors sought when sad36% seek odorous objects when they are sad (7% at least two, 29% one)� 27% seek objects involving social odors (15% attachment object), 5% food-related odors, 4% nature

odors, 5% other *6-Treasured odorous objects

34% treasure an odorous object (6% at least two, 28% one)� 9% cosmetics, 9% ambient fragrances, 9% scented toys/accessories, 9% objects carrying social odors,

3% other *7-Outside odors

74% would be annoyed in the absence of odors outside, it would suit 5%, 21% would not care

8-Smelling school tools32% smell school tools (11% often, 21% sometimes)

� 23% smell pens/pencils, 13% sheets/books, 4% glue, 4% eraser, 4% plastic tools, 7% other *

9-Odors in cars71 % are aware of an odor in their parents’ car

38% have positive reactions to this odor, 25% negative reactions, 8% indifferent

10-Odor of bathroom objects45% of the cited objects are considered as odorous (N = 1632 cited objects)� 28% of the odorous objects are soap/shampoo, 17% furniture/installations, 16% toothbrush/paste,

12% linen, 11% perfume, 16% other (N = 690 odorous objects)15-Tobacco smell

90% have negative reactions to the smell of tobacco smoke, 4% positive reactions, 6% indifferent

AO 96% are concerned by the owning of an AO (68% have one, 28% had one)� 79% of the AO are cuddly toys, 13% pieces of cloth, 7% dolls, 1% other (N = 248 cited objects)

27% of the children react to the odor change after washing (20% positive reactions, 7% negative reactions)18% direct their AO into the oro-nasal field

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Table 2. Gender, age, and verbal fluency effects on the 16 separate item scores of the COBEL, related to food, social and environmental odors. * p < .05, ** p < .01, *** p < .001

Items Gender effect1 Age effect2 Verbal fluency effect3

Food 1-Odor in food dislikes ns ���� *** ns

2-Response to unknown food ns ns ns

16-Guessing food odor ns � * ns

Social 11-Family odors f > m ** ns ns

12-People’s natural odor ns � ** f+ > f- **13-Smelling clothes f > m *** ns ns

14-Smelling self-odor f > m ** ns ns

Envir. 3-Senses in nature f > m ** ns f- > f+ * 4-Yesterday odors ns ���� *** f+ > f- **5-Odors sought when sad f > m *** ns ns

6-Treasured odorous objects f > m * ns ns

7-Outside odors ns ns ns

8-Smelling school tools ns ns ns

9-Odor in cars f > m ** ns ns

10-Odor of bathroom objects f > m ** � * ns

15-Tobacco smell ns ns ns1 Mann-Whitney U-tests (m/f: males/females)2 Kruskal-Wallis variance analyses (�: increase with age)3 Mann-Whitney U-tests (f+/f-: fluent/less fluent children)

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Table 3. Significant links between the variables related to the attachment object AO and the total and item scores of the COBEL (all the behaviors related to the attachment object are linked to higher scores). * p < .05, ** p < .01.

Separate item scores2

Variables related to the AO

Total COBEL score1 3-

Senses in nature

4-

Yesterday odors

5-

Odors sought

when sad

7-

Outside odors

12-

People’s natural odor

14-

Smelling self-odor

Having an AO(N = 206 vs. 9)

* **

Reacting to the odor change after washing (N = 59 vs. 156) * * **

� Reacting negatively to the odor change(N = 16 vs. 199)

* * ** *

Oro-nasal habits with the AO(N = 38 vs. 177)

* ** **

1 T-tests2 Mann-Whitney

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