Infants in control: rapid anticipation of action outcomes in a gaze-contingent paradigm.

Abstract

Infants' poor motor abilities limit their interaction with their environment and render studying infant cognition notoriously difficult. Exceptions are eye movements, which reach high accuracy early, but generally do not allow manipulation of the physical environment. In this study, real-time eye tracking is used to put 6- and 8-month-old infants in direct control of their visual surroundings to study the fundamental problem of discovery of agency, i.e. the ability to infer that certain sensory events are caused by one's own actions. We demonstrate that infants quickly learn to perform eye movements to trigger the appearance of new stimuli and that they anticipate the consequences of their actions in as few as 3 trials. Our findings show that infants can rapidly discover new ways of controlling their environment. We suggest that gaze-contingent paradigms offer effective new ways for studying many aspects of infant learning and cognition in an interactive fashion and provide new opportunities for behavioral training and treatment in infants.

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Infants in Control: Rapid Anticipation of Action
Outcomes in a Gaze-Contingent Paradigm
Quan Wang1, Jantina Bolhuis2, Constantin A. Rothkopf1, Thorsten Kolling2, Monika Knopf2, Jochen Triesch1*
1Frankfurt Institute for Advanced Studies, Frankfurt, Germany, 2Department of Psychology, Goethe-University Frankfurt, Frankfurt, Germany
Abstract
Infants’ poor motor abilities limit their interaction with their environment and render studying infant cognition notoriously
difficult. Exceptions are eye movements, which reach high accuracy early, but generally do not allow manipulation of the
physical environment. In this study, real-time eye tracking is used to put 6- and 8-month-old infants in direct control of their
visual surroundings to study the fundamental problem of discovery of agency, i.e. the ability to infer that certain sensory
events are caused by one’s own actions. We demonstrate that infants quickly learn to perform eye movements to trigger
the appearance of new stimuli and that they anticipate the consequences of their actions in as few as 3 trials. Our findings
show that infants can rapidly discover new ways of controlling their environment. We suggest that gaze-contingent
paradigms offer effective new ways for studying many aspects of infant learning and cognition in an interactive fashion and
provide new opportunities for behavioral training and treatment in infants.
Citation: Wang Q, Bolhuis J, Rothkopf CA, Kolling T, Knopf M, et al. (2012) Infants in Control: Rapid Anticipation of Action Outcomes in a Gaze-Contingent
Paradigm. PLoS ONE 7(2): e30884. doi:10.1371/journal.pone.0030884
Editor: Olaf Sporns, Indiana University, United States of America
Received August 29, 2011; Accepted December 29, 2011; Published February 17, 2012
Copyright: ? 2012 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the Bundesministerium fu ¨r Bildung und Forschung (http://www.bmbf.de/) project ‘‘Bernstein Focus: Neurotechnology
Frankfurt, FKZ 01GQ0840’’ and by the European Union (http://ec.europa.eu/research/fp7/) under grant IM-CLeVeR, FP7-ICT-IP-231722. The funders had no role in
study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: triesch@fias.uni-frankfurt.de
Introduction
As an infant tries to make sense of the vast array of signals from its
sense organs and wins control over its body and physical
environment, one of its most fundamental problems is to learn which
sensory events are the consequence of its own motor actions and
which ones are not, in other words, to discover agency. It has been
difficultsheddinglightonthisabilityininfantsbecauseoftheirlimited
motor repertoires [1,2]. Fortunately, however, infants reach accurate
control over their eyes comparatively early [3,4], suggesting that eye
movements could be used as a window into their ability to discover
novel action outcomes. Using a newly-developed gaze-contingent
(GC) paradigm employing automated eye-tracking, we here show
that6and8-month-oldinfantsreadilylookattargetstotriggercertain
sensory events and that they rapidly anticipate the outcomes of their
actions. In contrast to previous paradigms for studying infant
cognition based on looking behavior [5–12], our paradigm gives
infantsdirectcontroloverthephysicalenvironment,allowingthemto
change what is ‘‘out there’’ with their eye movements. Such gaze-
contingent paradigmsbased on eye-tracking have been explored with
adult subjects before [13], but only recently it has become possible to
apply eye tracking to infants [12,14]. The ability of infants to quickly
discover new ways of controlling their environment that we
demonstrate here, paves the way for truly interactive new paradigms
forstudyinginfantlearningandcognitionandmayprovideabasisfor
novel training and medical intervention strategies.
Results
In Experiment 1, infants learned to look at a red disc on a
screen in order to trigger the appearance of animal pictures (Video
S1). Subjects were twenty-four 6-month-olds (17 female, 7 male)
and six 8-month-olds (3 female, 3 male). The computer screen
initially displayed only the red disc (Fig. 1). By looking at this
‘‘button’’ the infant triggered a brief ‘‘bing’’ sound as well as the
appearance of an animal picture, which was displayed adjacent to
the red disc. Sound and picture occurred with a delay of 600 ms
after the infant had looked at the disc. The animal picture stayed
on the screen for 1.5 s before it disappeared and the infant could
trigger the button again after one second to drive the appearance
of a new animal picture.
Within a minute infants frequently ‘‘clicked’’ the button, with 8-
month-olds doing so significantly more often than 6-month-olds
(Fig. 2A, one-way-ANOVA, p=0.017). An analysis of fixation
durations on the button vs. the animal pictures revealed that
infants exhibited longer fixations on the animal pictures although
these were only present for brief 1.5 s intervals, while the button
was present for the entire duration (Fig. 2B, two-tailed t-test,
p=0.0004). This suggests that infants did not merely look at the
button because it was highly salient per se, but because they
wanted to trigger its function of producing a new animal picture.
To further investigate this issue, we analyzed the reaction times of
infants to see if they were predicting the appearance of the animal
picture. To this end the start time of the gaze shift bringing their
eyes to the area of the new animal picture was compared to the
onset time of the picture. The standard criterion of labeling gaze
shifts as anticipatory if they start within 200 ms of the picture onset
was applied [8]. Infants of both age groups had 48% of
anticipations according to this criterion. When comparing the
reaction times of the first click to the subsequent two clicks, we
found that infants across both age groups showed a significant
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decrease in reaction time (one-way ANOVA, Dunnet post hoc
p=0.037). Linear and inverse linear trend lines were fitted
revealing decreased average reaction times with increasing
number of clicks (Fig. 2C). This suggests that infants rapidly
discovered the contingency between looking at the button and the
appearance of a new picture. There were large individual
differences in reaction times, however. Figure 3 shows reaction
times of four representative infants showing very many to no
anticipations. Overall, the distribution of infants’ reaction times
had a bimodal structure with a strong peak for reactive saccades
and a smaller one for anticipatory saccades and was well fit by a
Gaussian mixture model (Fig. 4). In sum, our data show that most
infants produced gaze shifts anticipating the consequence of their
new form of agency within a few trials.
In Experiment 1, infants might have merely looked at the red
disc because it was the only stimulus left on the screen once an
animal picture had disappeared. To address this issue, we designed
a second experiment with two modifications. First, two identical
red buttons were displayed on either side of the screen. A small
cross was added to the red buttons to direct infants gaze towards
their center. Importantly, only one of the buttons had the function
of triggering the sound and the appearance of a new picture
(Fig. 5). The side of the functional button (left or right) was
counterbalanced across subjects. Second, the animal picture did
not disappear after 1.5 s but slowly faded out over an interval of
17 s. Thus, after the first click, the screen generally contained
three objects: the functioning and non-functioning buttons and the
fading animal picture. The latency between the triggering of the
functioning button and the appearance of a new picture was
450 ms, somewhat shorter than for Experiment 1.
Subjects were seventeen 6-month-olds (7 female, 10 male) and
sixteen 8-month-olds (7 female, 9 male). We also recruited a group
of twenty-five adult participants (20 female, 5 male, average age 26
years, range 19 to 49 years). The adult participants (without
instructions) were tested with the same experimental procedure as
the infants. The experiment ended when thirty pictures had been
seen or 5 min had passed. Subsequently, adult subjects filled in a
questionnaire testing their understanding of the function of the two
buttons. Somewhat surprisingly, the questionnaires revealed that
only 9 adults (36%) fully understood the function of the buttons.
We divided the adults into two corresponding groups, solvers and
non-solvers. For both groups we evaluated the distribution of click
intervals, i.e., the periods between subsequent clicks on the
functioning button (Fig. 6A, B). Click intervals of adult solvers
were significantly different from those of the adult non-solvers
(Wilcoxon rank sum test, p=1.65e-20), with only the adult solvers
showing many click intervals shorter than 10 s. Interestingly, the
data of the infants (Fig. 6A) closely match the data of the adult
solvers who had understood the function of the buttons (p=0.35),
but differs significantly from the data of the adult non-solvers
(p=2.1e-29). To test for specific differences in the usage of the two
buttons we further analyzed eye movements by considering the
frequency of two gaze patterns: a sequence of saccades leading
from the picture area to the (non-)functioning button and back to
the picture area was labeled a (non-)functioning-button-pattern.
Both the infant group and the adult solvers showed a significant
preference for the functioning-button-pattern over the non-
functioning-button-pattern (Fig. 6C; paired-sample t-test, infants,
p=0.042; adult solvers, p=0.006). This was not the case for the
adult non-solvers (Fig. 6C; p=0.885).
Discussion
Our data suggest that 6 and 8-month-old infants can quickly
discover novel forms of agency. They learn to manipulate their
environment using their eyes in a gaze-contingent (GC) paradigm
by selecting fixation targets that produce certain sensory outcomes
and they rapidly anticipate the outcomes of their actions. Previous
approaches to studying instrumental conditioning in infants were
limited by the comparatively crude and stereo-typed motor skills
that they considered including sucking and leg kicking [1,2]. The
central advantage of the GC paradigm is that it taps into a large
repertoire of discernible actions (eye movements to various objects
or locations, or possibly eye blinks) that infants can perform
Figure 1. Design and timing of Experiment 1.
doi:10.1371/journal.pone.0030884.g001
Figure 2. Results of Experiment 1. (A) Average click counts of 6-
month-olds and 8-month-olds. (B) Average fixation durations on image
area and button area. (C) Average reaction time as a function of click
number (error bars indicate s.e.m.). Only the first 15 clicks were plotted,
since only a minority of infants performed 16 or more clicks. Infants’
average reaction time after their first click is 277 ms, but becomes much
faster by the third click. A linear curve (y=27.53*x+218.77, R2~0:26)
and an inverse curve (y=123.5/x+158.35, R2~0:34) were fitted to
infants’ average reaction times.
doi:10.1371/journal.pone.0030884.g002
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accurately at a very young age. With our method we could
demonstrate rapid anticipation of action outcomes in infants as
young as 6 months, while the earliest previous report of such
behavior was a recent study showing 10-month-olds anticipating
the consequence of a manual button press [15]. Our findings also
raise many further questions. For example, how will these results
vary as a function of infant age or the delay between looking at the
button and the onset of sound and picture? More generally, our
method provides a paradigm to effectively investigate central issues
of discovery of agency and instrumental learning in infants. In an
independent recent study of Deligianni et al. [16], an experimental
condition has been realized in which a presented object became
animated when an infant fixated this object long enough, giving
another example of how gaze contingency can be used in infancy
research.
It is interesting to note that in Experiment 2 our group of 6- and
8-month-old infants performed better than the large group of adult
non-solvers. We speculate that the adult subjects have learned over
many years that just looking at inanimate objects does not produce
any effects in the external world. Infants, however, lack this
extensive experience and may be more ready to infer a causal
connection between their looking and changes in their physical
environment.
What may be the physiological basis of the learning processes
leading to the discovery of agency? We speculate that infants’
ability to rapidly anticipate the consequences of their actions may
be related to a recent proposal that the short-latency dopamine
signal, which is triggered by unexpected salient sensory events,
serves the discovery of novel actions [17]. In our paradigm such a
signal might be triggered by the initially unpredicted appearance
of the animal pictures evoked by eye-movements acquiring the
button. Further experiments are needed to shed light on this issue.
Note that such a mechanism for discovering agency may also play
a central role in mastering social interactions, where the infant
needs to discover that its caregivers and other conspecifics react
contingently to its behavior [18].
In general, GC paradigms based on eye tracking technology
may have a number of advantages compared to classic non-eye-
tracking paradigms for studying infant learning and cognition.
First, they extract very rich and detailed behavioral data. Second,
they allow studying various aspects of infant cognition in an
interactive fashion, giving young infants, who are very restricted
by their language and motor abilities, the possibility to
communicate with and act on the outside world. Third, by
putting infants in control of their environment, GC paradigms are
likely more engaging and satisfying for the infant. In fact, infants
displayed frequent signs of positive affect in the experiments. The
lower attrition rates in infant-controlled over experimenter-
controlled habituation paradigms [19] are also suggestive of a
greater satisfaction in paradigms where the environment reacts
contingently on the infant. Fourth, the use of GC paradigms may
allow testing young infants in adaptations of many classic
instrumental learning paradigms used in the animal learning
literature. Fifth, GC paradigms may be used to train cognitive
Figure 3. Individual reaction times in Experiment 1. Each subplot represents one individual. Six-month-olds are plotted in blue, eight-month-
old in red. Dashed horizontal lines are the anticipation threshold of 200 ms. There was no systematic difference between age or gender groups. Four
representative individuals were selected and ordered based on their average reaction times. (A) Very frequent anticipations. (B) Frequent
ancitipations. (C) Few anticipations. (D) No anticipations.
doi:10.1371/journal.pone.0030884.g003
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abilities in infants [20], allowing early intervention in populations
at risk. For these reasons, we expect to see many new GC
paradigms in infancy research in the future.
Materials and Methods
Families were recruited from a database of parents who had
expressed an interest in participating in research by calling back in
response to an information flyer distributed locally. The Ethics
Committee of the German Psychological Society only requires
ethical approval for interventional studies that involve potential
harm to the subject. In this study, no intervention was applied on
Figure 4. Three-component Gaussian mixture model fitted to reaction times. We found a strong component corresponding to reactive
gaze shifts (mean 230 ms, variance 66 ms2, explaining 53% of the data), a weaker component for anticipations (mean 2204 ms, variance 103 ms2,
explaining 14% of the data), and a third component of much larger variance covering outliers (mean 219 ms, variance 348 ms2, explaining 33% of the
data).
doi:10.1371/journal.pone.0030884.g004
Figure 5. Design and timing of Experiment 2.
doi:10.1371/journal.pone.0030884.g005
Figure 6. Results of Experiment 2. (A) Click interval distribution of
infants. (B) Click interval distribution of adult solvers (red) and non-
solvers (black). (C) Pattern count of infants, adult solvers and adult non-
solvers (blue: functioning-button pattern, red: non-functioning button
pattern).
doi:10.1371/journal.pone.0030884.g006
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the subjects as the task only involved looking at a computer screen,
as a result no ethical approval was necessary. Informed written
consent was obtained by all parents. Infants received a small toy
for their participation. All infant participants were healthy and
their birth week, weight, and Apgar-score reached standard values
[21]. Infants were tested within 10 days of their 6-month or 8-
month birthday.
Experiments were performed in a darkened and sound-
attenuated room, with the eye tracker screen as the only source
of lighting. Infants sat in an infant-seat (Weber Babyschale, http://
www.weber-products.de) placed on their parent’s lap. An EyeLink
1000 remote eye-tracking system was used (SR Research, http://
www.sr-research.com). The eye tracker camera was attached
underneath a 17 inch computer screen, and recorded the
reflection of an infrared light source on the cornea relative to
the pupil at a frequency of 500 Hz. The experimenter controlled
the stimulus presentation from a display computer in an adjacent
room while monitoring the infants behavior through a video
camera. The eye-tracker allowed for moderate head movements
without accuracy reduction in a volume of 22 cm618 cm620 cm
(horizontal6vertical6depth). Blink or occlusion recovery was
faster than 3 ms.
During the calibration process, attractive balls (shrinking from
approx. 2.50to a point) with sound were presented in a three-point
calibration sequence for infants, and a five-point-calibration was
used with adults. The calibration procedure was repeated if
necessary. Calibration procedures, stimulus presentation and data
output were accomplished using Experiment Builder software and
allowed an optimal accuracy of 0.5 degrees. The x, y coordinates
(in pixel) of the three point calibration positions on a screen
resolution of 10246768 were: (511.5, 65.2), (961.6, 701.8) and
(61.4, 701.8), for five point calibration they were (395.5, 287.5),
(395.5, 526.1), (359.5, 48.9), (675.9, 287.5) and (43.1, 287.5). A
human observer pressed a key when the participant was judged to
be fixating the stimulus at each location, and an exclusion criterion
was a 1.5 degree average error during validation of the calibration,
which corresponded to a 1.5 cm area on the screen with a viewing
distance of about 60 cm.
Animal pictures were taken from Animal Diversity Web (http://
animaldiversity.ummz.umich.edu). In Experiment 1, the size of
the pictures was 13.80horizontally; the red disc was 6.10, and the
distance between the border of the picture and the border of the
disc was 10.10. In Experiment 2, picture width was 12.40
horizontally, each disc’s radius was 5.40, and distances between
edge of picture and edge of discs were 3.90on both sides. Interest
areas for eye tracking analysis were defined to exactly match
position and size of the red discs and images.
Exclusion conditions were if a participant did not finish 1 min in
Experiment 1 or 3 min in Experiment 2 because of fuzziness,
excessive movement, sleeping, bad calibration, or software failure.
Data analysis was performed with EyeLink DataViewer software
and Matlab. In Experiment 1, dropout rate was 14% (5 infants).
Three subjects were excluded because of bad eye tracker
calibration, one because of fuzziness, and one because of a
software problem. In Experiment 2, dropout rate was 35% (18
infants). Fourteen infants were excluded because they did not
finish 3 min because of fuzziness, excessive movement, or sleeping,
three infants because of bad calibration, and one because of a
software problem. Adult dropout rate was 11% (3 adults), because
of poor eye tracker calibration.
For each data sample, the eye tracking software computed
instantaneous velocity and acceleration and compared these to
velocity and acceleration thresholds. If either was above threshold,
a saccade signal was generated. The Default Cognitive Configu-
ration was applied. Saccade velocity threshold was 30 deg/s and
saccade acceleration threshold was 8000 deg/s2. Eye position,
pupil size, velocity, etc. were updated every 50 ms during a
fixation.
In Experiment 1, anticipatory gaze shifts were identified as
follows. Gaze shifts from the button area to the picture area could
be composed of an individual saccade or a rapid sequence of two
saccades. In both cases, we considerd the start time of the first
saccade leaving the button area as the start time of the gaze shift.
We only considered situations where the start time of the gaze shift
occurred at least 200 ms after the previous image had disappeared
to rule out the possibility that the gaze shift was aimed at the
previous image. A gaze shift was considered anticipatory if its start
occurred within 200 ms of the onset of the new image.
Supporting Information
Video S1
iment 1.
(WMV)
Eye movement record of an infant in Exper-
Acknowledgments
The authors thank Kira Kastell, Peter Redgrave, Wolf Singer, Linda
Smith, and Rachel Wu for comments on earlier versions of the manuscript.
Zhenwen Dai provided code for fitting the mixture of Gaussian model.
Competing Interests: The authors declare that they have no competing
financial interests.
Author Contributions
Conceived and designed the experiments: QW JB CR TK MK JT.
Performed the experiments: JB. Analyzed the data: QW JB. Wrote the
paper: JT QW. Designed the software for the experiments: QW.
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