mise à jour du
1 janvier 2007
BMC Neurosci
2003; 24;4:33
The temporal relationship between reduction
of early imitative responses
and the development of attention mechanisms
Nakagawa A, Sukigara M, Benga O
The School of Humanities and Social Sciences, Nagoya City University, Japan
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To determine whether early imitative responses fade out following the maturation of attentional mechanisms, the relationship between primitive imitation behaviors and the development of attention was examined in 4-month-old infants. They were divided into high and low imitators, based on an index of imitation. The status of attention was assessed by studying inhibition of return (IOR). Nine-month-old infants were also tested to confirm the hypothesis.
Results: The IOR latency data replicate previous results that infants get faster to produce a covert shift of attention with increasing age. However, those 4-month-olds who showed less imitation had more rapid saccades to the cue before target presentation.
Conclusion: The cortical control of saccade planning appears to be related to an apparent drop in early imitation. We interpret the results as suggesting a relationship between the status of imitation and the neural development of attention-related eye movement.
Meltzoff and Moore [1] studied imitation by showing human neonates some adult facial gestures. Imitative responses were frequent at birth and decreased at approximately 2- to 3-months of age [2-4]. Bower [5] gave neonate imitation as an example of repetitive processes in development, in which the infant acquires certain skills, loses them and then acquires them again as s/he grows. In spite of the fact that the imitation ability manifests itself at birth, it soon seems to disappear, reappearing only toward the end of the child's first year. To date, although the literature contains some accounts of the dropout of neonate imitations [2,6,7], the question has not been explored from the standpoint of developmental neuroscience.

Rizzolatti et al. [8] speculated that a "mirror" mechanism, similar to that for a particular class of visuomotor neurons, could represent the simplest neural mechanism for many behaviors, such as imitative behaviors. These neurons, originally discovered in the ventral premotor cortex of monkeys, discharge both when the monkey performs a particular action and when it observes another individual making a similar action [9]. Thus, the neural "mirror" mechanism might allow a direct matching between the action observation and its execution. Various findings support the existence of this mechanism in humans [10,11]. Rizzolatti et al. [8], for example, refer to these behaviors represented by a "mirror" mechanism as "resonance behaviors", in which an individual reproduces overtly or internally an action similar to that of another individual. Two types of resonance behaviors were distinguished. The first type is that in which an individual repeats overtly a movement made by others in a quasi-automatic way. The second type is that in which the activation of neurons coding motor actions occurs in response to an observed action, but the observed action is not generated overtly. Its purpose is to generate a representation of the goal of an action. Neonate imitation, together with the fixed action patterns of birds and adult actions related to emotional life, is thought to belong to the first type [8].

A typical example of a resonance behavior of the above-mentioned first type is the imitative behavior of animals observed on particular occasions. As the best studied example, Rizzolatti et al. [8] give the behavior displayed by shore birds when alarmed. Typically, one or a few birds start flapping their wings, then others start reproducing it and, consequently, the whole flock flies away. However, an important difference was suggested between this contagious behavior of birds and neonate imitation, one of the human resonance behaviors of the first type, namely, the control mechanisms storing the externally evoked response and inhibiting its emission [8]. These could be present in humans as well as in most evolved species of animals. Imitation behavior of infants might also occur, because these control mechanisms are not mature. Typically adults do not repeat overtly an observed action.

Neuropsychologists have identified several imitative behavioral syndromes in adults. Lhermitte [12] has described imitation behavior as a clinical sign associated with a frontal lobe damage, suggesting that a release of a covert resonance phenomenon could be inhibited by frontal cortical areas in adults. Recent functional neuroimaging studies also indicate a top-down effect on the brain regions related to motor resonance in adults [11]. In other words, early imitation may disappear after infancy following the development of cortical control.

On the other hand, the control mechanisms which store the responses and delay repetition appear to be already present in infants, although their cortical mechanisms are immature [8]. The neural basis for imitation in the newborn population has not been frequently studied [11], but it has been proposed that the child's early imitation uses mainly subcortical regions including the superior colliculus via multimodal sensory mapping [13]. Accordingly, before cortical development, some subcortical mechanisms of inhibition could be related to the early control or reduction of imitative responses.

The present study examines the hypothesis that early imitative responses disappear following the maturation of a form of inhibition. By observing eye movements, we examine visual attention, which has several maturing aspects at four months of age, including the ability to disengage and move to a stimulus and the ability to inhibit. To assess the status of inhibition, we study inhibition of return (IOR) which is a bias against reorienting attention to a recently attended location [14]. This inhibitory aftereffect encourages orienting towards novel locations and makes search of the environment more efficient [15]. It is suggested that IOR is an attentional process and that the superior colliculus is involved in its manifestation [16,17]. It is reported to develop rapidly between 6 and 16 weeks [18].

The original design provided 4-month-old infants with both IOR and facial imitation tasks. Additionally, 9-month-olds were assessed in order to explore the relationship between the infant imitation and the maturation of a form of inhibition. Nine months is considered to be a major transition point of visual attention [19]. Besides, at 9 months, but not before, infants begin to tolerate longer delays between initial exposure to the action of others and subsequent tests of recall [20]. In a pilot study, we found that it was extremely difficult to make socially adept 9-month-olds focus on a single elementary act, for example, a mouth opening. Thus, for assessing imitation at 9 months, we decided to conduct the immediate imitation task on objects, instead of the facial imitation task. Nine-month-olds were reported to be able to imitate certain simple actions with novel toys immediately [20]. On the other hand, as nine-month-olds were reported to be able to perform deferred imitation on objects successfully [20], in other words, inhibit an observed action, the less immediate imitation we could observe, and the more mature form of inhibition subjects showed.

Since the development of attention is thought to have a relationship with individual differences in temperament [21], mothers of all infants filled out the Infant Behavior Questionnaire Revised (IBQ-R). The IBQ-R is a caregiver or parent report for assessing individual differences in emotional and motor reactivity and self-regulation [22]. The link between early imitative tendencies and temperament was suggested by Field [23].
Facial imitation behavior
The pilot study suggested that the facial gesture of the experimenter was less able to keep the 4-month-old infant's attention when seated semiupright in a baby chair. Therefore, the infant was placed on a small bed (70 cm ? 120 cm ? 40 cm) in the supine position. No subject could turn over in bed. The experimenter bent forward and faced the infant at a distance of approximately 30 cm. The second experimenter videotaped the subject's reactions using a portable digital video recorder (DCR-TRV30) from above the infant's head at an angle of approximately 60 degrees. He zoomed in on the infant's face, monitoring by means of the liquid crystal picture provided by the recorder. A research assistant reported the elapsed time, and her voice report was also recorded by the same video recorder.
When awake and calm, the infant was placed on the bed. A research assistant attracted the infant's attention by calling his/her name. Once the subject fixated on the experimenter, the observation period (60 sec) began when the experimenter presented a passive face (lips closed, neutral facial expression) to the infant. This established the baseline (B) for recording the infant's spontaneous gestures. Following this, the first gesture (mouth opening or tongue protrusion) was presented by the experimenter approximately four times in a 15-sec period. If the subject turned his or her gaze away from the experimenter, the subsequent gesture was not presented until the subject's attention again returned to the experimenter. This modeling period (M) was extended within this single presentation, until the subject was judged to be attentive to the stimulus four times. After this modeling period, the subject was allowed a 30-sec response period (R), during which the experimenter wore a passive facial expression. A second and different gesture was presented using the same procedure approximately 30 sec after the response period for the first one. The two facial gestures were modeled in random order.

Infants' responses were coded in random order by two scorers who were thoroughly familiar with the scoring system but blinded to the modeling. The scorer viewed the videotapes at a speed of her own choosing (from real time to frame by frame) and recorded all instances of infant mouth openings and tongue protrusions every three seconds. We referred to the previous studies for operational definitions for recording [2,7]. A mouth opening was defined as a separation of the lips, which is initiated by a drop of the jaw from a closed position. For infants who always maintained a small crack between their lips, the minimum separation of the lips during the baseline was defined as a closed position. Yawning was not included as an adequate mouth opening response. Tongue protrusion was defined as protrusion of the tip of the tongue beyond the back margin of the lower lip. It was also scored when the tongue moved forward in the open mouth but not beyond the lips. To make it easier to determine imitative behavior in the 4-month-old infants, we did not consider the quality of the responses (e.g., full or partial reproductions). A coincidence between reported frequencies every three seconds of two coders was evaluated with Peason's correlation coefficient. The r is .58 (N = 162, p < .001).

The total frequency of each relevant behavior was obtained for the modeling & responding and baseline periods. An index of imitation was constructed from these frequencies exploratively. It was computed by subtracting the number of target gestures per second produced during the baseline period from the number of those gestures per second produced during the modeling & responding period.

As the positive number (>0) indicates that infants show imitative behaviors, the larger the positive number is, the stronger the imitative tendency is.