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DOI: 10.1177/1745691611427305
2012 7: 18 Perspectives on Psychological Science
Bruno Laeng, Sylvain Sirois and Gustaf Gredebck
Pupillometry: A Window to the Preconscious?

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Perspectives on Psychological Science
7(1) 18 27
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The measurement of the diameter of the eyes pupils (in short,
pupillometry) within psychology just celebrated 50 years.
Researchers have firmly established that the pupil changes
size not only in response to changes in ambient light
(the pupillary light reflex), but also to significant nonvisual
stimuli as well as thoughts and emotions (Goldwater, 1972;
Loewenfeld, 1993). Although psychologists have made spo-
radic attempts to measure changes in the diameter of the pupil
prior to 1960 (e.g., Berrien & Huntington, 1943; Watson,
1916), a study by Hess and Polt (1960) represents the turning
point for establishing the method within the psychological
research community (Andreassi, 1995). Hesss study mea-
sured pupillary sizes of male and female adults while they
viewed photographic semi-nudes of adults of both sexes as
well as pictures of babies. As one could predict, the pupils of
both male and female observers dilated (of about 20% of the
diameter compared to baseline) when they viewed images of
half-naked members of the opposite sex, whereas only the
female observers shows significant dilations to pictures of
babies. A few years later, it became clear that pupillary
responses do not only constitute a response to arousing
or emotionally relevant stimuli (e.g., Aboyoun & Dabbs,
1998; Bernick, Kling, & Borowitz, 1971; Hamel, 1974; Hess,
Seltzer, & Shlien, 1965; Peavler & McLaughlin, 1967), but
could also express other fundamental cognitive mechanisms.
For example, increasing load on memory, by increasing the
span of a string of digits to be remembered, positively corre-
lated with pupillary size (Beatty & Kahneman, 1966). A few
years earlier, Hess and Polt (1964) similarly demonstrated that
difficulty of mental calculations (e.g., multiplication) corre-
lated positively with the size of the pupil (see also Ahern &
Beatty, 1979). In Kahnemans (1973) words, the eyes pupil
seemed to provide a window on the intensive aspect of
attention (i.e., its capacity, distinct from its selective
aspect), an often overlooked attentional variable within the
cognitive sciences. Similar suggestions have been brought for-
ward more recently. Just and Carpenter (1993) described the
pupillary response as an indicator of how intensely the pro-
cessing system is operating.
Kahnemans (1973) account of the pupillary response as an
index of load on attentional capacity is still useful, as many
subsequent studies have clearly shown a relationship between
pupillary dilation and executive load or working memory load
(e.g., Ahern & Beatty, 1979; Chatham, Frank, & Munakata,
2009; Hyn, Tommola, & Alaja, 1995; Kahneman & Peavler,
Corresponding Author:
Bruno Laeng, Department of Psychology, University of Oslo, 1094 Blindern,
0317 Oslo, Norway
E-mail: bruno.laeng@psykologi.uio.no
Pupillometry: A Window to
the Preconscious?
Bruno Laeng
1
, Sylvain Sirois
2
, and Gustaf Gredebck
3
1
Department of Psychology, University of Oslo,
2
Universit du Qubec Trois-Rivires, and
3
Uppsala University
Abstract
The measurement of pupil diameter in psychology (in short, pupillometry) has just celebrated 50 years. The method
established itself after the appearance of three seminal studies (Hess & Polt, 1960, 1964; Kahneman & Beatty, 1966). Since then,
the method has continued to play a significant role within the field, and pupillary responses have been successfully used to
provide an estimate of the intensity of mental activity and of changes in mental states, particularly changes in the allocation
of attention and the consolidation of perception. Remarkably, pupillary responses provide a continuous measure regardless
of whether the participant is aware of such changes. More recently, research in neuroscience has revealed a tight correlation
between the activity of the locus coeruleus (i.e., the hub of the noradrenergic system) and pupillary dilation. As we discuss in
this short review, these neurophysiological findings provide new important insights to the meaning of pupillary responses for
mental activity. Finally, given that pupillary responses can be easily measured in a noninvasive manner, occur from birth, and can
occur in the absence of voluntary, conscious processes, they constitute a very promising tool for the study of preverbal (e.g.,
infants) or nonverbal participants (e.g., animals, neurological patients).
Keywords
attention, consciousness, development, infant, methodology, neuroscience, neuroscience, unconscious/automatic processing
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Pupillometry 19
1969; Karatekin, Couperous, & Marcus, 2004; Nuthmann &
van der Meer, 2005; Piquado, Isaacowitz, & Wingfield, 2010;
Stanners, Coulter, Sweet, & Murphy, 1979; Van Gerven, Paas,
Van Merrinboer, & Schmidt, 2004; V et al., 2008) and inter-
ference or competition between stimuli and/or responses (e.g.,
Laeng, rbo, Holmlund, & Miozzo, 2011; Moresi et al., 2008;
Siegle, Ichikawa, & Steinhauer, 2008; Van der Meer et al.,
2003). Figure 1, for example, illustrates how the pupillary
response is clearly sensitive to the congruency effect of the
classic Stroop color-naming task.
However, recent evidence from pupillometry studies within
psychology and neuroscience indicates that the pupillary
response might offer a wider window on cognition than previ-
ously thought. Specifically, it may provide an index to pro-
cesses that occur below the threshold of consciousness.
Through the Eye to the Brain
Pupillary measurements
The size of the pupil of the eye is determined by the tone of
two muscles, the dilator and the constrictor; thus, a pupillary
dilation can be the result of a stimulation of the dilator or an
inhibition of the constrictor. In dim light or darkness, the pupil
can enlarge to an average size of about 7 mm with a standard
deviation (from this average) of about 0.9 mm (MacLachlan &
Howland, 2002); in standard light conditions, its average size
is about 3 mm (Wyatt, 1995). Thus, changes in illumination
can provoke pupillary dilations of more than double its typical
size (about 120%). Changes that are cognitively driven are
more modest and are rarely greater than 0.5 mm (Beatty &
Lucero-Wagoner, 2000). Thus, the pupillary response to sex-
ual stimuli, as originally measured by Hess and Polt (1960),
approximated the maximal dilation (a 20% change) that can be
elicited by psychologically relevant stimuli that are invariant
in luminance.
Pupillary responses occur spontaneously and they are dif-
ficult to control voluntarily. Specifically, a pupillary dilation
may be voluntarily provoked only in an indirect manner by
mentally imaging an object or event that would normally
evoke a pupillary dilation (e.g., sexual imagery; Whipple,
Ogden, & Komisaruk, 1992). However, it is impossible to sup-
press a pupillary dilation at will, whether it is provoked by
external stimuli or mental events (Loewenfeld, 1993). Pupil-
lary dilations evoked by psychologically relevant stimuli
occur as the result of a neural inhibitory mechanism on the
parasympathetic oculomotor complex or EdingerWestphal
nucleus by the noradrenergic systems locus coeruleus (LC;
Wilhelm, Wilhelm, & Ldtke, 1999).
Norepinephrine and the LC
The LC is a subcortical brain structure that constitutes the nor-
adrenergic systems hub to the whole brain (Aston-Jones &
Cohen, 2005; Sara, 2009). The LC is found on each side of the
rostral pons in the brainstem and gives rise to the sole source
of the neuro-transmitter norepinephrine (NE) to the cortex,
cerebellum, and hippocampus. The LC may be most known
among clinical psychologists for its role in syndromes like
clinical depression, panic disorder, and anxiety (e.g., Carter
200
200
400 600 800 1,000 1,200 1,400 1,600 1,800 2,000
ms
0.02
0.02
0.04
0.06
0.08
0.10
0.12
0.14
0.16
0.18
m
m
Congruent
Incongruent
Non-color words
Fig. 1. Mean pupil diameters (in mm) for each distractor condition during the classic color-word
Stroop interference task (from Laeng et al., 2011). Time 0 represents the onset of each stimulus, and
pupil size was sampled every 20 ms. The colored vertical lines represent the point in time of each
conditions mean reaction time. Pupillary responses clearly lag behind each explicit response (a key
press indicating the color of the word), but they showed the same pattern of results across conditions
(i.e., larger responses for incongruent combinations of pixel colors and color words than for the
congruent combinations).
by guest on March 28, 2014 pps.sagepub.com Downloaded from
20 Laeng et al.
et al., 2010; Klimek et al., 1997). The LC is activated by stress
and responds to it by increasing NE secretion through the
hypothalamicpituitaryadrenal axis and by altering the activ-
ity of prefrontal cortex. In addition, the LC is engaged during
the process of memory retrieval (Sterpenich et al., 2006) and
slow-wave sleep (Eschenko & Sara, 2008), suggesting a role
of the LCNE system in the consolidation of memories. At the
same time, the LC sends its densest innervations to brain areas
known to be involved in selective attention processing (e.g.,
parietal cortex, pulvinar nucleus, superior colliculus; Foote &
Morrison, 1987). One current hypothesis is that the noradren-
ergic system, which originates in the LC, mediates the func-
tional integration of the whole attentional brain system
(Corbetta, Patel, & Shulman, 2008; Coull, Bchel, Friston, &
Frith, 1999; Sara, 2009). Recently, Posner and Fan (2008)
have distinguished between alerting, orienting, and executive
networks of the brain. Within their model, the alerting network
is innervated by the NE system and includes the LC, right
frontal cortex, and regions of the parietal cortex. Within this
view, NE plays a crucial role in energizing the cortical system
and promoting adequate levels of activation for cognitive
performance.
What is most relevant for the present discussion about the
neurophysiology of pupillary response is that neuroscientists
have noted a very tight link between the online pupillary
response and the activation of the LC and NE system (Koss,
1986). The LC might be a key node within the neural circuitry
that also controls the muscles of the iris (Samuels & Szabadi,
2008), so that activity within this system gets reflected in the
dilation of the eyes pupil. The existence of such a relationship
allows researchers to map changes in LC activation through
pupil diameter, providing an externally observable response
that reflects activity of specific subcortical loci (Koss, 1986).
In addition, given that the LC is the key node of the noradren-
ergic system, pupillary responses can also be used to monitor
the activity of the NE system by simply observing relative
changes in pupil diameter or, in a metaphor, by using the natu-
ral pupillary resonance signal from the NE system. As such,
the connection between pupil diameter, the LC, and the NE
system allows researchers to measure pupil diameter in order
to tap changes in attention.
The above assumption is based on robust findings from
neuroscience that have established, by use of the single-cell
recording technique in monkeys, that changes in pupillary
diameter are tightly correlated to changes in activity in neu-
rons of the LC (Rajkowski, Kubiak, & Aston-Jones, 1993;
Rajkowski, Majczynski, Clayton, & Aston-Jones, 2004).
Figure 2 illustrates the close direct relationship between the
pupil diameter and baseline firing rate of LC neurons in the
monkey.
In the present review, we suggest that pupillary responses
can index changes in allocation of attention (a) when a con-
scious state about a stimulus or event is still in the making
(i.e., in a preconscious active state but unable to reach aware-
ness without top-down feedback; as defined by a recent theory
of consciousness by Dehaene, Changeux, Naccache, Sackur,
& Sergent, 2006), (b) when a conscious state remains incom-
plete (e.g., due to masking), or (c) cannot be made explicit
either via verbal or motor responses (e.g., in preverbal infants,
animals, and in some neurological patients). The above find-
ings should be viewed in the context of recent neurophysiolog-
ical evidence about the function of a small structure of the
brain: the LC.
Phasic and tonic activity in the LC. According to Aston-
Jones and Cohen (2005), two different modes of LC activity
correspond to different patterns of an animals behavior. In the
phasic mode, LC cells exhibit activation when processing
task-relevant stimuli, and this mode of function is consistently
associated with high levels of task performance (Aston-Jones,
Rajkowski, Kubiak, & Alexinsky, 1994; Bouret, Duvel, Onat,
& Sara, 2003; Usher, Cohen, Servan-Schreiber, Rajkowski, &
Aston-Jones, 1999). In the tonic mode, LC cells fail to respond
phasically to task events, and the animals exhibit poor perfor-
mance on tasks that require focused attention and show an
increase in distractibility. However, the animal is more likely
to detect novel stimuli in the tonic mode. This dissociation in
functional modes points to two fundamental cognitive mecha-
nisms: A focused or exploitation mode that adaptively
adjusts attentional filtering to optimize performance during a
specific task or event, and a diffuse or exploration mode
that adaptively adjusts the scope of attention to optimize shifts
of performance between tasks or events (see Table 1).
If LC tonic activity favors exploration and abandoning a
current task for another, whereas LC phasic activity signals the
occurrence of task-relevant events, then we would expect
pupillometry studies to reveal the same relationship between
tonic and phasic pupillary changes in humans during the same
conditions. An ample variety of studies have consistently
0 2,000 4,000
Time (s)
1.0
1.5
Constrict
Dilate
L
C

N
e
u
r
o
n

(
H
z
)
P
u
p
i
l

D
i
a
m
e
t
e
r
Fig. 2. The above curve shows pupil diameters as taken by a remote eye-
tracking camera while a monkey fixed gaze on a spot of light during a signal-
detection task. The curve below displays the baseline firing rate of an LC
neuron while it was recorded from an electrode simultaneously to the
pupillary responses. The two measurements are shown phased-locked to one
another (from Aston-Jones & Cohen, 2005).
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Pupillometry 21
shown that processing task-relevant events is time locked to
rapid (phasic) and dramatic pupillary dilations (Beatty,
1982; Kahneman & Peavler, 1969; Poock, 1973; Richer &
Beatty, 1985; Simpson, 1969). For example, when participants
are asked to report the presence of a visual target during rapid
serial visual presentation, pupil dilation is significantly associ-
ated with target detection, and its amplitude reflects the fre-
quency of targets and the time of the detection (Privitera,
Renninger, Carney, Klein, & Aguilar, 2008). Indeed, any stim-
uli that have some relevance to the observer are likely to pro-
voke a pupillary response in the form of dilation (e.g., Hess
et al., 1965, Hess & Polt, 1966; Janisse, 1974; Kuchinke,
Trapp, Jacobs, & Leder, 2009; Libby, Lacey, & Lacey, 1973;
Partala & Surakka, 2003).
Tonic changes in pupillary diameter have been investigated
less than have changes that are time locked to the presentation
of specific stimuli (i.e., event-related stimuli), despite the rel-
evance of the brains tonic activation in Posners (1992, 1993)
neural model of attention. Nevertheless, several studies con-
verge to a similar relationship between pupillary tonic response
and task difficulty, mental effort, and the state of arousal or
vigilance of the participants. Sustained processing yields an
increase in the pupil tonic response (e.g., Siegle et al., 2008).
As difficulty and/or arousal increases, performance gradually
degrades and large increases in pupillary baseline are concom-
itantly observed (Beatty, 1982; Granholm, Asarnow, Sarkin, &
Dykes, 1996; Howells, Stein, & Russell, 2010; Lavie, 1979;
Peavler, 1974; Verney, Granholm, & Marshall, 2004). Con-
versely, when the tonic state is low, as in a person who is
fatigued after sustained attention or is sleepy, the pupil begins
to fluctuate considerably while its average diameter gradually
decreases (Beatty, 1982; Karatekin, Marcus, & Couperous,
2007). Indeed, the pupillographic sleepiness test has been used
as an objective alertness test in European sleep research and
sleep medicine (Wilhelm, Widman, Durst, Heine, & Otto,
2009; Wilhelm, Wilhelm, Ldtke, Streicher, & Adler, 1998).
Thus, the existing models of LC function (Aston-Jones &
Cohen, 2005; Yu & Dayan, 2005) predict changes in both
baseline- and stimulus-related pupil diameter in tasks in which
both the difficulty and reward values of the task are concur-
rently manipulated. Specifically, the model of Aston-Jones
and Cohen (2005) correctly predicted that, in a tone discrimi-
nation task, human pupillary responses would reveal large
phasic dilation for each discrimination but that these dilations
would decrease in amplitude as difficulty increased while
baseline (tonic) pupil diameter increased and peaked at the
time participants decided to abandon the task and reset dif-
ficulty to a lower level. Yu and Dayan (2005) proposed a
Bayesian model of LC function, according to which a change
in the environment (or an unexpected uncertainty) leads to a
revision of an organisms optimal inferences and such a pro-
cess is modulated by NE release by the LC.
Current models of the attention network in the human
brain. The fact that the LC plays a key role in both focusing
attention and disengaging ongoing action/thought is, in itself,
a good neurophysiological premise for using the pupil as a
window to changes in states of consciousness (Bouret & Sara,
2005). Attention and consciousness are intimately related,
although they have not the same function and may depend on
different cerebral processes and structures (Koch & Tsuchiya,
2006).
The influential biased-competition model of attention
(Desimone & Duncan, 1995) proposes that objects in a visual
scene compete for access to working memory and that atten-
tion is biased by top-down (volitional) signals that promote the
selection of relevant objects. These top-down signals in work-
ing memory interact with the salient bottom-up signals of
objects in the visual scene, so that the most relevant objects are
selected attentively and thus perceived while unimportant
objects are confined to a negligible status (Bundesen,
Habekost, & Kyllingsbk, 2005; Wolfe, 1994, 2006).
Recently, two attentional systems have been distinguished
(Corbetta et al., 2008): a selection system centered on the dor-
sal portions of the parietal and frontal cortex responsible for
the selection of sensory information and responses (Vanden-
berghe, Gitelman, Parrish, & Mesulam, 2001), and a detection
system, centered on the ventral portions of the temporo-pari-
etal and frontal cortex responsible for the detection of relevant
events, particularly salient and unattended stimuli (Raizada &
Poldrack, 2008). The latter, ventral detection system might be
most relevant for the type of information that is picked up by
pupillary changes as this network receives strong input from
the LCNE system.
Specifically, the LC phasic signal has been conceptualized
as an interrupt signal or as a network reset signal (Bouret
& Sara, 2004; Dayan & Yu, 2006) that allows the network to
detect a new target or event. Neuroimaging studies of healthy
humans suggest a functional relationship between signals of
the LC and activity in the ventral attention network (Corbetta
et al., 2008), both in relation to attentional transitions (tonic
signals) and target detection (phasic response). The LC has a
latency to a stimulus of about 100150 ms, and the transmis-
sion of its output to the cortex is of about 50100 ms, which
would allow a highly synchronized LC activation of the ven-
tral attentional network, which in turn would allow the dorsal
network to switch to and consolidate ones perception into
another more appropriate state (Yantis & Serences, 2003).
Table 1. Performance Level in Perceptual or Cognitive Tasks
as Predicted From an Animals Engagement in Each of Two
Fundamental Modes of Attention and by Two Fundamental
Neuronal Activation Modes of the Locus Coeruleus
Modes of locus
coeruleus activity
Modes of attention
Focused exploitation Diffuse exploration
Phasic High performance Poor performance
Tonic Poor performance High performance
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22 Laeng et al.
Indeed, a decrease in tonic LC activity is observed whenever
subjects engage in a demanding task, reflecting a top-down
filtering signal that restricts the attentional focus to a narrow
range of relevant events that are contingent to a task or mind
set. Conversely, the high tonic LC activity is hypothesized to
correspond to an exploratory, broad sensitivity mode to either
external or internal (mental) events.
The pupil as a marker of attentional shifts. Recent studies
of conscious perception have capitalized on the fact that some
visual stimuli can give rise to different, often incompatible,
perceptions. Some of the first examples of such images were
Jastrows duck-rabbit, the Rubins vase-faces, and the so-
called Necker cube. These bistable images as well as over-
lapping images seen in binocular rivalry (i.e., when two
completely different images are presented simultaneously but
separately to each eye) are characterized by a conscious per-
ception that oscillates in time between two different interpreta-
tions of the same image so that sustained stimulations can
result in repeated and rapid shifts between one conscious
image or the other (Tong, Nakayama, Vaughan, & Kanwisher,
1998). During changes in perception, nothing changes in the
world or environmental input, so any change in perception
must be attributed to an internal change of state of the brain
that results in interpreting the same world-state as a different
event.
What is most interesting is that monitoring pupillary
responses can reveal the brains detection of such event bound-
aries evoked by the bistable image of the Necker cube
(Einhuser, Stout, Koch, & Carter, 2008). Specifically,
Einhuser and colleagues (2008) asked their participants to
report the time of perceptual switching by pressing a button.
As shown in Figure 3, it was found that the pupil diameter
significantly increased around the time of the perceptual
switch and that the period of significantly larger dilations from
baseline occurred within the time range of () 244 ms before
and (+) 1552 ms after the reported switch with maximal peak at
(+) 602 ms. Because a percepts dominance duration (i.e., how
long one of competing percepts lasts) can fluctuate considerably
between conditions, participants, and even within a trial, Ein-
huser and colleagues calculated a normalized measure of post-
switch duration relative to the corresponding preswitch duration,
so that Point 0 of Figure 3 corresponds to equal durations before
and after switches. Figure 3 also illustrates how the rate of
increase in pupil dilation was maximal around the time of the
switch in awareness and started just before its report. Finally,
the larger the pupillary dilation around the time of the change in
perception, the more stable the subsequent perception.
As Einhuser et al. (2008) also point out, their results are
highly consistent with the previously sketched account by
Aston-Jones and Cohen (2005), in which the pupillary
response indicates LCs activity and NE levels in the brain in
modulating between exploitation (e.g., continue what you are
doing) and exploration (e.g., disengage and choose between
one of the alternative possibilities). Moreover, the physiolog-
ical plausibility of such an account is also strengthened by the
consideration that, in monkeys, the LC phasic response occurs
about 100 ms after a relevant event (e.g., a target stimulus sig-
naling a reward) and it takes an additional 6070 ms for the
activity within the LC nucleus to reach frontal cortex and
about 100 ms for it to reach the occipital cortex. Such a delay
from the triggering event to NE release at a cortical site is then
about 150200 msa time course that is well within the range
required for NE to plausibly have an influence on the crucial
cortical network before the manual report of the change in per-
ception. Although additional studies will be necessary to clar-
ify the extent to which the pupillary response correlates to
perceptual dynamics (see Hup, Lamirel, & Lorenceau, 2009),
the above evidence strongly suggests that pupillary responses
could provide an easily observable signal of the moment in
which one event becomes relevant and consolidates into
awareness, whereas alternative events are discarded and then
eventually consigned to a negligible status.
The Preconscious Pupil
Stimuli presented at the visual threshold (i.e., barely percepti-
ble) tend to provoke significant pupillary dilations when they
are detected (Hakerem & Sutton, 1966). However, recent stud-
ies with normal participants have also revealed that the pres-
ence of subliminal reward cues can trigger pupillary dilations
that are proportional to the cues value as well as the level of
demands of a costbenefits, decision-making task (Bijleveld,
Custers, & Aarts, 2009). A study of Laeng and Falkenberg
(2007) showed that women maximally dilated their pupils
when passively viewing photographs of their boyfriends dur-
ing the ovulatory (fertile) stage of their cycle, despite these
hormone-based changes in motivational state typically going
unnoticed by these participants. It would then seem that
0.8
0
0.4
3 +3 0
Time to Report [s]
P
u
p
i
l

D
i
a
m
e
t
.

[
z
]
n = 398
p < .014
Fig. 3. Pupil diameter during the perceptual rivalry task produced by
observing the Necker cube shape and reporting each reversal at the time
of its occurrence by pressing a switch button. The pupil diameter scores are
normalized to z scores and aligned to time of reported switch; means and
standard errors were pooled across all switches of all subjects. The bottom
horizontal black line denotes a period significantly different from 0 (from
Einhuser, Stout, Koch, & Carter, 2008).
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Pupillometry 23
pupillary dilations could also reflect changes of motivational
state that occur below the threshold of perceptibility.
Weiskrantz, Cowey, and Barbur (1999) pointed out that the
pupillary response, being nonverbal, lends itself particularly
well to the investigation of residual visual capacity in neuro-
logical patients that these patients themselves may not be
aware to have retained. Patients with damage to the visual cor-
tex (V1) often show blindsight; they can correctly guess about
stimuli that they do not see (Weiskrantz, 1990, 1998) because
the stimuli appear within their area of blindness. For example,
in patients who suffered localized brain damage to V1, it is
still possible to measure a reliable constriction of the pupil to
spatial gratings presented within the blind field (Weiskrantz,
Cowey, & Le Mare, 1998). The occurrence of the phenomenon
of blindsight is supposedly based on processing by alternative
neural pathways that bypass V1. Weiskrantz et al. (1999)
found that the pupillary constriction response could be due to
particular visual properties of gratings appearing and disap-
pearing suddenly within the blind field, regardless of whether
the patients reported any awareness of them. They concluded
that although the pupillary response indirectly indexes a pro-
cess that signals defensive and alerting reactions to stimuli that
move rapidly and appear suddenly (e.g., events of special
importance or danger), awareness is clearly not a necessary
accompaniment to the presence of such a response.
Most remarkably, another study with blindsight patients
showed that emotional faces seen within the blind area could
provoke appropriate emotional responses from the patients
(Tamietto et al., 2009). Specifically, the patients showed a
spontaneous tendency to synchronize their facial expressions
(i.e., a phenomenon known as emotional contagion) to the
subliminal facial expressions shown within their blind area.
Moreover, the pupillary responses showed larger dilation to
the arousing value of the invisible emotional expressions.
Another study, this time with amnesic patients with damage to
the hippocampus (Laeng et al., 2007), has shown a remarkable
ability of patients to discriminate novel stimuli from old ones,
as revealed by their pupillary dilations to the new stimuli,
despite the severe explicit memory problem and the total
absence of an explicit discrimination between novel and the
previously attended stimuli.
A constructive manner to interpret the unusual dissociations
shown by these neurological patients is that some brain areas,
including the amygdala, can process the stimuli but, without the
support of cortical processes underlying a top-down attentional
amplification of the represented information as well as recurrent
loops of activity or functional connectivity between multiple
areas (Dehaene et al., 2006; Lamme, 2006; Tononi, Sporns, &
Edelman, 1992), a consciously accessible percept cannot be
established. Normally, the information processed by these brain
structures would be in a potential state of becoming an object of
awareness and, indeed, the role attributed to several subcortical
structures, like the amygdala and LC, is precisely that of warn-
ing and alerting the (primarily frontal) cortical areas to switch
the course of current processing so as to give relevance to new
stimuli or events or objectives (Duncan & Barrett, 2007; Gompf
et al., 2010; Laeng et al., 2011; Liddell et al., 2005; Sterpenich
et al., 2006). If, as a result of neurological damage, the workings
of these areas remain isolated or functionally disconnected, then
necessarily their information will remain confined to a poten-
tial state that cannot be completely accessed. In other words,
information that would be normally in a preconscious status
would, in these pathological conditions, remain unconscious
although still capable of influencing behavior, decisions, and
emotional responses.
Indeed, the term preconscious has recently reappeared within
the psychological taxonomy (Dehaene et al., 2006; see also
Kihlstrom, 1995). The term was originally used by Freud (1900)
for potential contents of awareness; that is, knowledge or mem-
ories that are not presently conscious but that are accessible in
principle (Laplanche & Pontalis, 1973). In Dehaene and col-
leaguess (2006) tripartite model of conscious, preconscious,
and subliminal processing, the preconscious state is a tran-
sient one in which information is potentially accessible, yet not
accessed. Chapman, Oka, Bradshaw, Jacobson, and Donaldson
(1999) already explicitly suggested that the cognitive aspects of
the pupillary response are preconscious; that is, the pupil can
indicate the presence of processing that takes place before con-
scious perception and that may be necessary for phenomenal
awareness (cf. Block, 2005).
Developmental Pupillometry
Studying developmental populations most often require
unique research paradigms that are not dependent on language
or complex behavioral responses. For infant studies, this often
means measuring the change in overall looking time from one
stimulus set to another (habituation) or infants preference for
one stimulus over another (preferential looking). For a discus-
sion about the limitations of these measures, see Aslin (2007).
For infant researchers, the analysis of pupillary responses
allows novel questions about attentional states and precon-
scious processes that are either time locked (phasic) or con-
tinuous (tonic) over longer periods of time. To date, some
initial studies have been carried out, suggesting that pupillary
responses might be a robust and sensitive measure well suited
for preverbal populations.
Early studies on infants (Fitzgerald, 1968; Fitzgerald, Lintz,
Brackbill, & Adams, 1967; see Goldwater, 1972) observed
greater pupillary dilation to pictures of faces than to geometric
shapes, which is reminiscent of the early study by Fantz, Ordy,
and Udelf (1962) on preferential looking of neonates on faces.
Fitzgerald (1968) also found that the picture of the babys
mother provoked greater pupillary dilation than did a picture
of a stranger. However, the method used involved infrared
film running at 2Hz and measuring by the diameter of the
pupil by hand on a projection screen for each frame. This was
tedious, expensive, and provided coarse data, which is possi-
bly why (to the best of our knowledge) there was a 30-year gap
before pupillometry was used again in infancy research.
by guest on March 28, 2014 pps.sagepub.com Downloaded from
24 Laeng et al.
Following this intermission, it has been demonstrated that
pupillary responses differ as a function of age and of the spa-
tial properties of grating stimuli in infants between 1 and 3
months of age (Cocker & Moseley, 1996). The amplitude and
latency of light adaptation responses also decrease with
increased postgestational age in prematurely born infants
(Cocker, Fielder, Moseley, & Edwards, 2005).
In recent years, researchers have begun to revisit the con-
nection between phasic pupillary responses and psychological
processes that goes beyond vision. Jackson and Sirois (2009)
demonstrated that 8-month-old infants react with larger pupil
dilations after having observed a physically impossible event
(one train entering a tunnel and another train exiting the same
tunnel) relative to a more conventional physical event (the
same train entered and exited the tunnel). Although pupil
diameter proved a much finer discriminant variable relative to
the traditional looking time measure, Jackson and Sirois
(2009) found no correlation between look duration and peak
pupil diameter. This finding invites further investigation given
the important methodological implications it may have for the
field. At the same time, Gredebck and Melinder (2010) used
pupil dilation to assess infants reactions to violations of nor-
mal social interactions. In this case, both 6- and 12-month-old
infants dilated their pupils more after having observed irratio-
nal than rational feeding actions (for recent studies with older
children, see Anderson, Colombo, & Shaddy, 2006; Chatham
et al., 2009; Falck-Ytter, 2008; Piquado et al., 2010).
These differential pupillary responses to surprising physi-
cal events (Jackson & Sirois, 2009) and irrational social inter-
actions (Gredebck & Melinder, 2010) might be related to
arousal and increased cognitive load. This article provides
three additional speculations that provide a plausible descrip-
tion of the underlying mechanisms. First of all, the connection
between arousal and/or cognitive load on one hand and pupil
dilations on the other appeared to be mediated by alterations in
the intensity of the attentional processing system (Ahern &
Beatty, 1979; Just & Carpenter, 1993; Kahneman, 1973). Sec-
ond, the phasic nature of infants reactions suggests that this
alternation is primarily related to focused attention. Third,
based on the adult and animal data reviewed above, it is fair to
assume that reactions are preconscious and mediated by acti-
vation within the LC and a surge of NE to the cortex.
Conclusions
Our goal in this article is to encourage researchers in several
and often separate fields to benefit from the use of pupillom-
etry. First of all, it is a relatively inexpensive method com-
pared to several other physiological methods (EEG, fMRI,
MEG) and it is completely noninvasive. An added advantage
is that pupillometry is usually obtained by use of an eye
tracker, and therefore it is often coupled to the acquisition of
other continuous measurements of ocular data like eye fixa-
tions and saccades, which can be phase locked to the unfolding
of cognitive processes. Thus, eye movements and pupillary
responses share the benefit of providing clues about the real-
time structuring of cognitive processing (cf. Richardson, Dale,
& Spivey, 2007; Spivey, 2007). In fact, pupil recording can
occur without any disruption of behavioral tasks and, as a non-
invasive measure, it does not require overt responses and can
be obtainable even without participant knowledge. Moreover,
researchers can also profit from the sensitivity of pupil varia-
tions to representations or responses that are only partially
activated and that may never pass the threshold for eliciting
overt behavior or conscious appraisal (Bijleveld et al., 2009;
Laeng et al., 2007). One potential application of pupillometry
could involve subjects that cannot normally understand
instructions or provide controlled, verbal responses (e.g.,
aphasic patients, patients with locked-in syndrome).
However, the greatest promise of pupillometry may lie in
its ability to reveal online processes that occur in experimental
subjects who are either preverbal (i.e., infants; Gredebck &
Melinder, 2010; Jackson & Sirois, 2009) or simply lack lan-
guage (e.g., animals; Iriki, Tanaka, & Iwamura, 1996). We
believe that a combination of the method with recent advances
in infancy research allow us to start asking serious questions
about consciousness early in ontology, and it may open an
entire new frontier of research within developmental cognitive
science and comparative psychology.
Declaration of Conflicting Interests
The authors declared that they had no conflicts of interest with
respect to their authorship or the publication of this article.
Funding
This article was funded by Grants VR-2009-1348 and VR-2011-1528
from the Swedish Research Council.
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