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.
