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Development and Psychopathology 21 (2009), 726

Copyright # 2009 Cambridge University Press


Printed in the United States of America
doi:10.1017/S0954579409000029

SPECIAL SECTION ARTICLE


Pubertal changes in emotional information
processing: Pupillary, behavioral, and
subjective evidence during emotional
word identification

JENNIFER S. SILK, GREG J. SIEGLE, DIANA J. WHALEN,


LAURA J. OSTAPENKO, CECILE D. LADOUCEUR, AND RONALD E. DAHL
University of Pittsburgh School of Medicine

Abstract
This study investigated pupillary and behavioral responses to an emotional word valence identification paradigm among
32 pre-/early pubertal and 34 mid-/late pubertal typically developing children and adolescents. Participants were asked to
identify the valence of positive, negative, and neutral words while pupil dilation was assessed using an eyetracker.
Mid-/late pubertal children showed greater peak pupillary reactivity to words presented during the emotional word
identification task than pre-/early pubertal children, regardless of word valence. Mid-/late pubertal children also showed
smaller sustained pupil dilation than pre-/early pubertal children after the word was no longer on screen. These findings
were replicated controlling for participants age. In addition, mid-/late pubertal children had faster reaction times to all
words, and rated themselves as more emotional during their laboratory visit compared to pre-/early pubertal children.
Greater recall of emotional words following the task was associated with mid-/late pubertal status, and greater recall
of emotional words was also associated with higher peak pupil dilation. These results provide physiological, behavioral,
and subjective evidence consistent with a model of puberty-specific changes in neurobehavioral systems underpinning
emotional reactivity.

This study examines puberty-related changes in opment may help us to understand a paradox
neurobehavioral systems underpinning emo- in adolescent health (Dahl, 2004; Steinberg
tional reactivity and regulation using pupillary et al., 2006). Although adolescence is one of
and behavioral measures of emotionally salient the healthiest periods of the life span with re-
information processing. Gaining a better under- spect to physical health, overall morbidity and
standing of normative changes in emotional mortality rates increase 200300% (Ozer, Mac-
information processing across pubertal devel- donald, & Irwin, 2002; Resnick et al., 1997).
Accidents, suicide, homicide, depression, anx-
We are grateful to Joanna Prout for her assistance in this pro-
iety, alcohol and substance use, eating disor-
ject. We also thank the participants and their families. This ders, human immunodeficiency virus, sexually
research was supported by National Institute of Mental transmitted diseases, and unwanted pregnan-
Health (NIMH) R24 Research Network Grant MH67346 cies all increase sharply in this developmental
(R.E.D., PI) and Grant K01 MHO73077 (J.S.S., PI). period (Ozer et al., 2002; US Preventive Ser-
Address correspondence and reprint requests to: Jenni-
fer S. Silk, Department of Psychiatry, University of Pitts-
vices Task Force, 1996). Furthermore, many
burgh School of Medicine, 3811 OHara Street, Pittsburgh, of the most costly, chronic, and impairing disor-
PA 15260; E-mail: silkj@upmc.edu. ders of adulthood, including mood disorders,

7
8 J. S. Silk et al.

anxiety disorders, and drug and alcohol abuse, risk and reward, may be directly linked to
typically onset during adolescence (Alpert, pubertal maturation (Nelson, Leibenluft, Mc-
Maddocks, Rosenbaum, & Fava, 1994; Chung, Clure, & Pine, 2005; Steinberg, 2007; Steinberg
Martin, & Winters, 2006; Pine, Cohen, Gurley, et al., 2006). These areas undergo significant
Brook, & Ma, 1998). reorganization in early adolescence that appears
Many of these problems and disorders have to be triggered, at least in part, by the hormonal
been linked to the onset of puberty or early pu- changes of puberty (see Nelson et al., 2005;
bertal maturation, particularly in females (An- Patton & Viner, 2007). Emerging evidence
gold, Costello, & Worthman, 1998; Caspi, from animal and human studies suggests that,
Lynam, Moffitt, & Silva, 1993; Ge, Conger, presumably as a result of this reorganization,
& Elder, 1996; Graber, Lewinsohn, Seeley, & the brain systems that regulate rewards, social
Brooks-Gunn, 1997; Orr & Ingersoll, 1995). information, and emotions become more sensi-
This puberty-linked increase in adolescent tive and/or active during puberty (Chambers,
mental and behavioral health problems appears Taylor, & Potenza, 2003; Dahl, 2001; Nelson
to be related to difficulties with the control of et al., 2005; Spear, 2000; Steinberg, 2005,
emotions and behavior (Dahl, 2004). In fact, 2007). Consequently, pubertal adolescents
many health problems that increase during seem to seek experiences that create high-inten-
this period involve dysregulation of emotion sity feelings. For example, one study found that
(e.g., bipolar disorder, depression, anxiety dis- among adolescents of a similar age, those who
order) or risk taking and poor decision making were more advanced in puberty were more
in the face of emotional influence (e.g., unsafe likely to seek exciting experiences and show
sex, peer pressure to engage in substance abuse risk-taking behavior (Martin et al., 2002). In ad-
or drunk driving). Consistent with this model, dition, Quevedo, Benning, Gunnar, and Dahl
there is initial evidence that problems in emo- (see this issue, 2009) found that pubertal ado-
tion regulation during adolescence are linked lescents showed appetitive potentiation of the
to the development of depressive symptoms postauricular reflex, a marker of appetitive mo-
and problem behaviors (Silk, Steinberg, & tivation, whereas their same-age prepubertal
Morris, 2003), although the role of puberty in peers showed no modulation of this reflex.
this relationship is not well understood. Thus, Quevedo et al. also found that puberty was as-
gaining a better understanding of normative sociated with an increase in the magnitude of
puberty-specific changes in systems involved the eye-blink startle response during an affec-
in emotional reactivity and regulation is critical tive picture viewing paradigm regardless of the
to elucidating the nature of adolescent health valence of the picture, suggesting that puberty
problems and refining prevention and interven- may be associated with a general increase in
tion approaches. the reactivity of neural systems underlying the
startle response, possibly including the amyg-
dala and fear-related circuitry.
Development of Neurobehavioral Systems
Increased sensation seeking and/or affective
Subserving Emotional Information
intensity could interact with the socialcon-
Processing During Adolescence
textual changes that accompany puberty to
Recent research in developmental neuroscience lead to a spiraling of both positive and negative
suggests that problems in emotion regulation emotions. The transition through adolescence
during adolescence may result from dyssyn- involves a period of flux and renegotiation
chronous development in neurobehavioral sys- (Cicchetti & Rogosch, 2002), including dra-
tems involved in both emotional reactivity and matic changes in the social environment, such
regulation (Dahl, 2004; Ernst, Pine, & Hardin, as the increasing importance of peer and ro-
2005; Steinberg, 2005; Steinberg et al., 2006). mantic relationships, changing family relation-
There is some evidence that change in regions ships, and entry into quasiadult roles such as
of the brain that subserve primarily socioemo- working and driving (Steinberg & Morris, 2000;
tional functions, such as responding to social Steinberg & Silk, 2002). Evidence suggests
stimuli, and the perception and evaluation of that changes in the parentchild relationship,
Puberty and pupillary reactivity 9

including increased frequency and intensity of the full capacity to regulate the associated emo-
parentadolescent conflict, may actually be di- tion. This has led to a metaphor for the histori-
rectly linked to pubertal maturation (Steinberg, cal advancement of puberty as starting the en-
1987). Other changes are indirectly triggered by gines with an unskilled driver (Dahl, 2004).
puberty because changes in physical appear- This dilemma may explain, in part, the fact
ance lead to changes in the way children and that adolescents often make poor decisions
adolescents are treated by parents, other adults, (e.g., high rates of participation in dangerous
and peers, especially those of the opposite gen- activities such as automobile accidents, drug
der. A wide array of affective challenges ac- use, and unprotected sex) despite understand-
company these new experiences, including in- ing cognitively the risks involved (Cauffman
creased self-consciousness, social anxieties, & Steinberg, 1995; Reyna & Farley, 2006; Slo-
igniting romantic interests, academic pressures, vic, 1987, 2000). These decisions may reflect
and attempts to balance a desire for immediate an imbalance in cognitive and emotional influ-
gratification with an understanding of the im- ences on decision making and behavior during
portance of long-term goals and consequences. adolescence, with the scale temporarily tipped
These changes can be both exhilarating and toward emotional influences until skills in cog-
overwhelming, creating new challenges in the nitive control gradually catch-up (Ernst et al.,
integration of cognitive and emotional pro- 2005).
cesses in ways that require skills in emotion Despite this compelling model, few empirical
regulation. studies have examined puberty-specific changes
Some evidence suggests that the adolescent in affective systems in human populations. There
brain may not be fully prepared to handle these is a need to better understand normative changes
challenges. Brain regions that subserve cog- in emotional information processing across pu-
nitive control functions mature more gradually bertal development (Steinberg et al., 2006). In
over the course of adolescence and young the current study, we address this question by
adulthood, and are believed to be largely inde- examining whether pubertal differences exist in
pendent of pubertal timing (Steinberg et al., pupillary reactivity to emotional stimuli among
2006). For example, regions of the prefrontal a sample of typically developing children and
cortex that underpin higher cognitiveexecutive adolescents.
functions show functional changes that continue
well into late adolescence and even early adult-
The Pupillometric Approach to Studying
hood (Jernigan & Sowell, 1997; Lewis, 1997;
Emotional Information Processing
Sowell & Jernigan, 1998). Perhaps as a result
of this continued maturation, adolescents appear Pupillometry is a novel approach to studying
to perform cognitive tasks less efficiently than emotional information processing that holds
adults (Luna et al., 2001) and utilize a different promise for understanding puberty-specific
set of brain structures than adults to accomplish changes in affective systems. An ancient pro-
certain attentional tasks in the context of emotion verb holds that the eye is the window to the
(Monk et al., 2003). soul. In fact, research suggests that the pupil
Thus, it is believed that puberty directly af- does provide a window into the activity of the
fects neural systems involved in social and mind. Pupil dilation provides a peripheral index
emotional responsivity, whereas development of brain activation in response to a specific
of systems mediating higher cognitive func- stimulus. The pupil becomes more dilated in re-
tions occurs slowly, continues well beyond sponse to stimuli that require greater cognitive
pubertal maturation, and is relatively indepen- load or that have greater emotional intensity
dent of pubertal timing (Dahl, 2004; Nelson (Beatty, 1982; Beatty & Lucero Wagoner, 2000;
et al., 2002). With pubertal onset occurring at Siegle, Steinhauer, Carter, Ramel, & Thase, 2003;
earlier ages (Herman-Giddens, 2006; Worth- Siegle, Steinhauer, & Thase, 2004). For example,
man, 1999), adolescents may now find them- research has carefully demonstrated incremental
selves in emotionally challenging situations as increases in pupil dilation with conditions requir-
much as a decade before having developed ing greater memory or cognitive effort, such
10 J. S. Silk et al.

as remembering more digits, up until a person recently shown renewed interest in utilizing
reaches the limits of his or her mental capacity the pupillometric approach in emotional infor-
(Granholm, Asarnow, Sarkin, & Dykes, 1996; mation processing paradigms. For example,
Kahneman & Beatty, 1966). Partala and Surakka (2003) found that the pu-
This response occurs because the pupil is in- pils of normal adults dilated more to positive
nervated by brain structures involved in both and negative sounds than to neutral sounds. In
cognitive and emotional processing. Inhibition a study using an emotion regulation paradigm,
of the constrictor muscle occurs through para- Urry et al. (2006) recently demonstrated that
sympathetic innervation of the Edinger Whest- when participants are asked to intentionally
phal nucleus, which receives extensive inputs regulate their affect, initial and sustained pupil
from cortical and limbic regions. Stimulation dilation is increased.
of the dilator muscle occurs through a hypothal- Siegle and colleagues (Siegle, Granholm, In-
amic pathway, which also receives corticolim- gram, & Matt, 2001; Siegle, Steinhauer, Carter,
bic inputs. Thus, stimulation of limbic regions et al., 2003) have shown that patterns of pupil
such as the amygdala increases pupil dilation dilation to emotional stimuli are altered in de-
(Koikegami & Yoshida, 1953), as does stimu- pressed adults relative to normal controls. For
lation of the midbrain reticular formation example, depressed adults show increased and
(Beatty, 1986). The midbrain reticular forma- sustained pupil dilation on a task requiring iden-
tion receives afferent projections from the fron- tification of the valence of emotional words for
tal cortex, particularly, structures such as the up to 30 s after their responses compared to nor-
anterior cingulate cortex, which are implicated mal controls. This finding has been replicated
in emotion regulation (Szabadi & Bradshaw, in both medicated and unmedicated adults
1996), and sends efferent projections to the with major depressive disorder (MDD), and has
ocular motor nuclei. Concurrent pupillary/func- been shown to be specific to emotional rather
tional magnetic resonance (fMRI) studies sug- than purely cognitive information processing
gest that pupil dilation provides a summative (Siegle et al., 2001, 2004, 2008). It is correlated
index of task-related cognitive/affective brain with self-reported rumination, and thus appears
activity (Siegle, Steinhauer, Stenger, Konecky, to reflect sustained elaboration on emotional
& Carter, 2003). Pupil dilation also provides in- information (Siegle, Steinhauer, Carter, et al.,
formation about the time course of brain activa- 2003).
tion in response to a stimulus. The pupil re- Although researchers have used pupil di-
mains dilated as long as the processing demand lation as an index of cognitive processing in
persists and, because pupil dilation can be sam- children and adolescents (Gardner, Philp, &
pled every 16 ms, provides a dynamic measure Radacy, 1978; Juris & Velden, 1977), we are
of changes in cognitive/affective load following only aware of one study that has used pupil-
exposure to the stimulus. lometry to examine emotional information pro-
Pupillometry has long been used in cog- cessing in children and adolescents. Silk et al.
nitive science to understand cognitive processes (2007) examined depressed and typically de-
(see Beatty & Lucero Wagoner, 2000). The role veloping childrens pupil dilation to emotional
of the pupil in emotional processing has also words on a valence identification task similar
been recognized for a long time (Janisse, to the task completed by depressed adults in
1973), although remarkably little research has Siegle et al.s (2001; Siegle, Steinhauer, Carter,
been conducted in this area. Early studies of et al., 2003) studies. We found that depressed
the pupillary response to emotion refuted the children and adolescents exhibited a dimin-
original theory put forward by Hess (1965) ished late pupil dilation response to negative
that the pupil dilates in response to attractive emotional words relative to controls that was
stimuli and constricts in response to aversive related to greater depressive severity. We also
stimuli, instead demonstrating that the pupil di- found that children with lower levels of late pu-
lates to both positive and negative emotional pil dilation to negative words in the laboratory
stimuli (Janisse & Peavler, 1974; Stelmack & reported experiencing higher levels of negative
Mandelzys, 1975). Emotion researchers have emotion, lower positive emotion, and a lower
Puberty and pupillary reactivity 11

ratio of positive to negative emotion in their ranged in age from 8.1 to 17.9 years (M 13.2,
everyday lives using ecological momentary as- SD 3.0). Thirty-four participants were in the
sessment, suggesting that the finding related to mid-/late pubertal group (ages 10.9617.91,
problems in emotion regulation in depressed M 15.43, SD 1.74), and 32 were in the
youth. These findings were unique to sustained pre-/early pubertal group (ages 8.0614.75,
processing. Overall, the Silk et al. (2007) find- M 10.83, SD 2.08). Figure 1 displays the dis-
ings suggested that depressed children might be tribution of age as a function of pubertal status
avoiding negative emotional information, group and additional demographic characteristics
blunting their emotional response, or engaging are presented in Table 1. Exclusion criteria for the
in less regulation in response to negative emo- study included: (a) symptoms suggestive of an
tional information. It is important that this pat- Axis I psychiatric disorder based on the Child
tern differed from Siegle et al.s (2001; Siegle, Symptom Inventory4 (CSI-4; Gadow & Spraf-
Steinhauer, Carter, et al., 2003) findings for de- kin, 1998b) or the Adolescent Symptom Inven-
pressed adults, which showed increased pupil tory4 (ASI-4; Gadow & Sprafkin, 1998a), (b)
dilation to negative words in depressed subjects the existence of a major systemic medical illness,
relative to controls. This discrepancy high- (c) a history of serious head injury, or (d) having
lighted the need for normative data on the de- eye problems or difficulties in vision not correc-
velopmental trajectory of pupillary reactivity ted by the use of glasses or contact lenses.
to emotional information, which the present
study was designed, in part, to address.
Procedure
The universitys institutional review board ap-
The Current Study
proved the study. All participants were recruited
This study investigates pupil dilation to emo- from community advertisements and normal
tional stimuli among a new sample of pre-/early control samples in existing research projects.
and mid-/late pubertal typically developing chil- To participate in the study, children and their
dren and adolescents in the seconds following parents were required to sign assents and in-
presentation of emotional words. We examined formed consents, respectively. Because this
initial pupillary reactivity to emotional words study focused on a normative sample of chil-
as well as sustained pupil dilation after the dren, participants psychiatric symptomatology
word was no longer on-screen. Because of theo- was assessed using a questionnaire that screens
rized increases in sensitivity to affective stimuli, for Diagnostic and Statistical Manual of
we hypothesized that mid-/late pubertal children Mental DisordersFourth Edition (DSM-IV;
would show greater initial pupillary reactivity to American Psychiatric Association, 1994) Axis
emotional words than pre-/early pubertal chil- I disorders, the CSI-4 or the ASI-4 (Gadow &
dren. We also conducted exploratory analyses Sprafkin, 1998a, 1998b), with the parent or
to examine whether sustained processing of guardian serving as the informant. Participants
emotional words differed across pubertal devel- completed an initial phone screen and one 2-hr
opment. Finally, we hypothesized that mid-/late laboratory visit at the Child and Adolescent
pubertal children would have a slower reaction Neurobehavioral Laboratory, during which
time to label the emotional words than pre-/early event-related potential and pupil dilation assess-
pubertal children because of emotional interfer- ments were completed using methods described
ence effects, and would rate themselves as more previously (Ladouceur et al., 2005; Siegle,
emotional during the laboratory visit. Steinhauer, Carter, et al., 2003; Silk et al., 2007).

Method Self-report measures


Current affect. The Positive and Negative Af-
Participants
fect Schedule for Children (PANAS-C; Laurent
Participants were 66 typically developing chil- et al., 1999) was used as a child-report measure
dren and adolescents. Participants (39 females) of current feelings of positive and negative
12 J. S. Silk et al.

Figure 1. The distribution of participants age as a function of the pubertal status group. [A color version of
this figure can be viewed online at journals.cambridge.org/dpp]

Table 1. Demographic characteristics of participants

Pre-/Early Pubertal Mid-/Late Pubertal


(n 32) (n 34) t /x 2

Sex (% female) 50.00 67.60 x 2 (1) 2.12


Ethnicity (% White) 77.40 88.20 x 2 (1) 1.35
SES (Hollingshead)
M 52.64 50.97 t (63) 0.66
SD 10.56 10.01
Age
M 10.83 15.43 t (64) 29.78**
SD 2.08 1.74
PDSa
M 1.91 3.29 t (49) 212.68**
SD 0.52 0.32

Note: SES, socioeconomic status; PDS, Pubertal Development Scale (Peterson et al., 1988).
a
See the revised PDS scoring criteria in the Method Section.
**p , .01.
Puberty and pupillary reactivity 13

affect at the beginning of the testing session. questions that met these criteria required partic-
Thirty emotions were rated on a 5-point scale, ipants to rate puberty-related physiological
with positive emotions summed to form a changes. The excluded questions asked for sub-
Positive Affect Scale and negative emotions jective measurements of height, weight, and
summed to form a Negative Affect Scale. The pubertal completion as well as the assessment
PANAS-C possesses high internal consistency of pubertal development in relation to peers.
and good convergent and divergent validity A composite measure was created on a 4-point
(Laurent et al., 1999). scale with a median score of 2.8. A median split
was used to place participants into pre-/early
Demographic information. A sociodemo- and mid-/late pubertal groups. These decisions
graphic questionnaire was used to obtain socio- were based on earlier studies in our laboratory
demographic information from parent and that included Tanner staging by physical
child. This questionnaire included information exam and hormonal measures of puberty in
regarding basic sociodemographic information conjunction with the PDS. The PDS has been
such as age, gender, family history of affective shown to correlate with Tanner stages on phys-
disorders, and socioeconomic status (Hollings- ical exam (Brooks Gunn, Warren, Rosso, &
head, 1975). Gargiulo, 1987). Recently, Shirtcliff, Heiligen-
stein, Hoornstra, Squires, and Pollack (2007)
Psychiatric symptomatology. To screen for found that the PDS was correlated with Tanner
Axis I psychiatric disorders in this normative stages based on physical exam and was also a
sample of children, parents completed a paper good predictor of basal hormones responsible
and pencil psychiatric screening inventory for advancing pubertal development.
about child symptomatology. Parents of chil-
dren 12 years of age and older completed the Pupil dilation assessment. The pupil dilation
ASI-4 (Gadow & Sprafkin, 1998a) and parents testing occurred in a moderately lit room in
of children less than 12 completed the CSI-4 which the experimenter was present. Stimuli
(Gadow & Sprafkin, 1998b). The ASI-4 and were displayed in dark gray on a light gray com-
CSI-4 both inquire about child behavior over puter screen. Participants sat approximately
17 categories related to DSM-IV (American 122 cm from the bottom of the stimulus. Stim-
Psychiatric Association, 1994) diagnostic cate- uli were lowercase letters approximately 1 cm
gories. The ASI-4 and CSI-4 demonstrate con- high, subtending a 458 visual angle. Reaction
vergent and discriminant validity with corre- times were recorded using a game pad capable
sponding scales of the Child Behavior of reading reaction times with millisecond reso-
Checklist (Achenbach, 1991) and with clini- lution. The game pad was modified to have
cian diagnoses (Gadow & Sprafkin, 1998a, only three working buttons, arranged in a trian-
1998b). The CSI-4 has also been shown to cor- gle, so that respondents fingers were nearly
relate with DSM-IV diagnoses (Gadow, Devin- equidistant from each possible response. To ac-
cent, Pomeroy, & Azizian, 2005). count for differential response latencies to dif-
ferent buttons, the mapping of game pad but-
Pubertal development. Pubertal status was mea- tons to responses was counterbalanced across
sured using the Pubertal Development Scale participants.
(PDS; Petersen, Crockett, Richards, & Boxer, Pupil dilation was recorded using methods
1988), a self-report measure of pubertal status previously described and tested (Siegle et al.,
completed by each child that has been shown 2001; Siegle, Steinhauer, Carter, et al., 2003).
to have good psychometric properties (Petersen In brief, data were collected using a table-
et al., 1988). To score the PDS, we only in- mounted RK-726 eyetracker. The eyetracker
cluded questions that indexed the three main consisted of a video camera and infrared light
developmental axes of puberty: growth (item source that were pointed at a participants eye
1), adrenal (items 2 and 3), and gonadal (items and a device that tracked the location and size
4 and 5, males only; item 6, females only; see of the pupil using these tools. Pupil size was re-
Dorn, Dahl, Woodward, & Biro, 2006). The corded at 60 Hz (every 16 ms) and passed
14 J. S. Silk et al.

digitally from the eyetracker to a computer that smoothed using a 10-point weighted average
stored the acquired data along with signals filter. Then, linear trends in pupil dilation calcu-
marking the beginning of trials, the end of fixa- lated over blocks of trials were removed from
tion, stimulus onset time, and reaction time. pupil dilation data to eliminate effects of slow
The resolution for a typical participant was bet- drift in pupil diameter not related to trial charac-
ter than 0.05-mm pupil diameter. teristics. The final pupil dilation variable used
in analyses was a measure of change in pupil
Word valence identification (VID) task and diameter from baseline calculated for each sam-
word recall. Pupil dilation was collected while ple (every 16 ms) and then averaged across
participants completed a word VID. Partici- samples for each second in a trial. Baseline pu-
pants were instructed to identify the emotional pil diameter was calculated separately for each
valence of 66 words by pressing a correspond- trial based on the average dilation over the
ing button as quickly and accurately as possible. 167 ms (10 samples) preceding the onset of
Using the three-button game pad described the stimulus. Baseline pupil diameter was sub-
above, participants pressed the button that cor- tracted from pupil diameter after stimulus onset
responded with their rating of the word as pos- to produce the final pupil dilation index. This
itive, negative, or neutral. The positive (i.e., index therefore represents a change in millime-
birthday), negative (i.e., divorce), and neutral ters from baseline. Pupil dilation was then aver-
(i.e., lamp) words used in the word VID task aged across seconds in a trial to create pupil
were chosen from a corpus of emotional words dilation waveforms depicting the average time
normed for use with children and adolescents course of pupil dilation across a 12-s trial by
(Neshat-Doost, Moradi, Taghavi, Yule, & Dal- word valence (positive, negative, or neutral)
gleish, 1999). Twenty-two words from each va- or puberty group.
lence category were selected and balanced for
word length and frequency. Each trial included
Plan of analyses
a 1-s fixation mask (a row of Xs that they were
instructed to look at), the presentation of the Pupil dilation analyses were conducted using
word for 5 s, and a mask (another row of Xs) mixed effects models with an autoregressive
for the 6-s intertrial interval. A word recall as- (AR1) covariance structure, using pupil dilation
sessment was administered following the as the dependent variable. Models included pu-
word VID task. Children were given 1 min pil dilation at each second for each valence per
and 30 s to recall as many of the words from subject, with subject treated as a random effect
the task as possible. For the purposes of this and time and valence as repeated measures.
analysis, we calculated indices of number of Fixed effects included pubertal group, valence,
emotional (positive or negative) and neutral waveform segment, and all interactions. Based
words recalled. on previous studies (e.g. Siegle, Steinhuer, Car-
ter, et al., 2003; Silk et al., 2007), we focused on
Data selection, cleaning, and reduction. Trials two specific regions of interest in the pupil dila-
with reaction times below 100 ms and above tion waveform: (a) a peak segment defined as
4.9 s were discarded as outliers (Matthews & the period 24 s following word presentation,
Southall, 1991). Data were cleaned using our and (b) a late segment defined as the latter
laboratorys standard procedures (derived 3 s of the period during which the word was
from Granholm et al., 1996). Blinks were iden- off-screen (912 s). The peak segment repre-
tified as large changes in pupil dilation occur- sents initial reactivity and the late segment
ring too rapidly to signify actual dilation or con- represents sustained processing. Because the
traction. Trials comprised of over 50% blinks pupil continues to grow throughout childhood
were removed from consideration. These proce- and adolescence, peaking somewhere between
dures resulted in the elimination of M 16 the ages of 6 and 20 (Boev et al., 2005; Kohnen,
trials per subject. Linear interpolations replaced Zubcov, & Kohnen, 2004; MacLachlan &
blinks throughout the data set. Data were Howland, 2002), baseline pupil size could
Puberty and pupillary reactivity 15

introduce a confound, as having a larger pupil 0.36) than pre-/early pubertal children (M
would allow for a greater range of reactivity. 2.53, SD 0.40) on a global measure of emo-
For this reason, we also included a covariate tionality that included the average of all positive
for baseline pupil diameter to account for po- and negative items on the PANAS-C.
tential differences in pupillary reactivity based Next, we examined participants harmonic
on differences in pupillary size across pubertal mean reaction times (time taken to classify
development. words) on the valence identification task to
To follow up significant effects from the test whether puberty groups differed in overall
mixed models, group and valence contrasts on reaction time or reaction time to words of a spe-
pupil dilation were examined at each sample cific valence. A repeated-measures analysis of
along pupil dilation waveforms. Guthrie and variance (ANOVA) indicated that there were
Buchwalds (1991) contiguity threshold tech- no differences in reaction times by word va-
nique was used to control type I error across these lence and no Pubertal GroupValence interac-
tests. This technique defines the size of a tem- tions, but mid-/late pubertal children responded
poral window over which a series of contiguous more quickly to all words (M 1,364.40,
point-by-point tests could be considered signifi- SD 274.65) than pre-/early pubertal children
cant, controlling error across all tests at p , .05. (M 1,769.94, SD 400.20).
Autocorrelation is accounted for via Monte
Carlo simulations of the maximum length of ad-
Pupil dilation
jacent significant tests present in less than 5% of
simulated data with a similar autocorrelation We examined pupil dilation waveforms to test
structure to acquired empirical data. Using this for group differences in pupil dilation during
technique, regions of the waveforms were con- the word VID task. Mixed effects analyses indi-
sidered significantly different when over 0.78 s cated a main effect on pupil dilation for word
of consecutive tests were statistically significant valence, F (2, 877) 3.44, p , .05, and a
at p , .1 in the peak (24 s) region and when main effect for waveform segment, F (1, 489)
over 0.95 s of consecutive tests were statistically 59.50, p , .001, that was qualified by a
significant at p , .1 in the late (912 s) region. Group  Segment interaction, F (1, 489)
4.64, p , .05. The GroupValenceSegment
interaction did not reach statistical significance,
Results
F (1, 922) 2.15, p .12. There was no effect
Table 1 shows demographic characteristics of of baseline pupil diameter on pupil dilation dur-
the sample. As shown in Table 1, there were ing the task, F (1, 394) 0.03, p .86.
no gender, race, or socioeconomic status differ- Pairwise comparisons of estimated marginal
ences between the pre-/early and mid-/late pu- means for the valence effect revealed that pupil
bertal groups. dilation across the waveform was greater to neu-
tral words (M 0.07 mm) than to positive
words (M 0.05 mm); however, this difference
PANAS-C ratings and reaction times
was not significant using Guthrie and Buch-
Table 2 presents comparison of puberty groups walds (1991) contiguity threshold criterion.
on behavioral and subjective measures. We first To follow up the Group  Segment interaction,
examined whether puberty groups differed on group contrasts on pupil dilation were exam-
self-reported emotionality in the lab. We found ined at each point along pupil dilation wave-
that mid-/late pubertal children rated their cur- forms within the peak and late regions. Results
rent negative affect on the PANAS-C higher of these analyses, shown in Figure 2, indicate
(M 1.82, SD 0.53) than pre-/early pubertal that pubertal groups differed in their peak pupil
children (M 1.58, SD 0.38). There were no dilation, with mid-/late pubertal children show-
significant differences in ratings of positive af- ing greater peak pupil dilation than pre-/early
fect on the PANAS-C, although mid-/late pu- pubertal children, regardless of word valence:
bertal children were higher (M 2.74, SD 1.78 to 2.93 s: t (64) 2.40, p , .05, d .59.
16 J. S. Silk et al.

Table 2. Pubertal differences in behavioral and subjective measures of emotional processing

Pre-/Early Pubertal Mid-/Late Pubertal


(n 32) (n 34) t Cohen d

PANAS-C
Positive 1.16 0.27
M 3.48 3.65
SD 0.73 0.49
Negative 2.07* 0.52
M 1.58 1.82
SD 0.38 0.53
Emotional 2.19* 0.55
M 2.53 2.74
SD 0.40 0.36
Word recall
Neutral 0.90 0.22
M 2.06 2.62
SD 2.37 2.64
Emotional 2.84** 0.70
M 5.72 7.94
SD 2.98 3.37
Reaction time
Positive 2.84** 1.27
M 1741.77 1311.92
SD 399.33 264.79
Negative 3.68** 0.90
M 1805.31 1395.56
SD 539.58 351.87
Neutral 4.52** 1.11
M 1762.73 1385.71
SD 380.44 294.31

Note: PANAS-C, Positive and Negative Affect Schedule for Children (Laurent et al., 1999).
*p , .05. **p , .01.

Pubertal groups also differed in late pupil dila- sufficient degrees of freedom to conduct ex-
tion, with mid-/late pubertal children showing ploratory analyses including both age and pu-
decreased late pupil dilation compared to berty. To do so, we recomputed the mixed ef-
pre-/early pubertal children in the final second fects model described above controlling for
of the task: 11.03 to 12.00 s: t (64) 22.05, participants age. The Pubertal Group  Seg-
p , .05, d 2.50. ment interaction remained significant control-
We also conducted exploratory analyses to ling for age, F (1, 489) 4.75, p , .05. Be-
examine specificity of these findings to puber- cause there was a significant main effect for
tal status. Because age is measured more pre- age, F (1, 397) 9.24, p , .01, we recomputed
cisely than puberty, it will typically wash out the mixed effects model using participants age
the effects of puberty when it is included in rather than pubertal status. This model included
the same model; thus, this is a conservative a random effect for subject, repeated effects for
analysis. However, the high number of degrees time and valence, and fixed effects for age, va-
of freedom provided by measuring pupil dila- lence, waveform segment, and all interactions,
tion repeatedly over time (one measurement as well as a covariate for baseline pupil diame-
per second for 12 measurements per participant ter. The effect for valence remained significant,
per condition), and the analysis of this data in a F (2, 877) 4.73, p , .01; however, the Age
mixed effects model accounting for temporal Segment interaction was not significant, F (1,
autocorrelation among measurements, yielded 489) 2.74, p .10. Furthermore, there were
Puberty and pupillary reactivity 17

Figure 2. Pubertal group differences in pupil dilation to all words. Shaded regions are statistically significant
at p , .05. [A color version of this figure can be viewed online at journals.cambridge.org/dpp]

not significant correlations between peak pupil Relations among pupil dilation and word
dilation and age (r .18, p .15) or between recall, PANAS-C ratings, and reaction time
late pupil dilation and age (r .02, p .88),
We examined relations between behavioral and
suggesting that the pupil dilation findings
subjective measures using bivariate correla-
were not driven by age.
tions. Table 3 shows intercorrelations among
PANAS-C ratings, reaction times, and partici-
pants word recall. These correlations reveal
Word recall
that current positive affect ratings on the
To examine whether word recall on the free re- PANAS-C were not related to other indices of
call test immediately following the word VID emotional information processing, but ratings
task was associated with pubertal status, we of current negative affect and overall emotion-
conducted a multinomial logistic regression to ality on the PANAS-C were associated with re-
predict puberty group membership from recall membering more emotional words on the free
of emotional and neutral words. Number of recall task. In addition, there were inverse rela-
emotional words recalled emerged as a predic- tionships between emotional words and reac-
tor of pubertal status (B 2.26, p , .01), tion time on all conditions of the task, with chil-
but not number of neutral words recalled (B dren who responded faster remembering more
2.15, p .18). Follow-up t tests indicated emotional words. Relationships between reac-
that mid-/late pubertal children remembered tion time and memory for neutral words were
more emotional words (M 7.94, SD 3.37) less strong, with significant associations be-
than pre-/early pubertal children (M 5.72, tween memory for neutral words and reaction
SD 2.98; t 2.84, p , .01). There were no times to positive words but not to negative or
differences in the number of neutral words re- neutral words. Together, the findings suggest
called by mid-/late pubertal children (M 2.62, that youth higher in emotionality had faster re-
SD 2.64) and pre-/early pubertal children action times on the word VID task as well as
(M 2.06, SD 2.37; t .90, p .37). biased memory for emotional words.
18 J. S. Silk et al.

Table 3. Intercorrelations between behavioral and subjective measures of emotional processing

PANAS WR RT

PA NA EMOT Neutral EMOT Positive Negative Neutral

1. PANAS PA
2. PANAS NA .02
3. PANAS EMOT .80** .62**
6. WR neutral .09 2.02 .06
7. WR EMOT .13 .25* .25* 2.15
8. RT positive 2.05 2.06 2.08 2.35** 2.40**
9. RT negative 2.07 2.03 2.07 2.22 2.40** .81**
10. RT neutral 2.05 .07 .09 2.14 2.38** .78** .78**

Note: PANAS, Positive and Negative Affect Schedule for Children (Laurent et al., 1999); PA, positive affect; NA, negative
affect; EMOT, emotional; WR, word recall; RT, reaction time.
*p , .05. **p , .01.

We also conducted exploratory analyses ex- Table 4. Bivariate correlations between


amining how the initial pupillary response was initial peak and late pupil dilation and
related to behavioral and subjective measures of behavioral and subjective measures
emotionality. As we needed a single peak value
for use in correlations, we extracted each partic- Pupil Dilation
ipants average peak pupil dilation. This was
Peak Late
computed by calculating the highest pupil dila-
tion value within the 2- to 4-s window for each PANAS-C
trial and averaging this peak value across trials. Positive .19 2.08
As puberty groups did not differ in pupil dila- Negative .02 .06
tion by word valence, peak pupil dilation was Emotional .17 2.03
Word recall
collapsed across word valence categories. Neutral 2.08 .17
Table 4 summarizes the correlations between Emotional .31* 2.03
peak pupil dilation and the behavioral and sub- Reaction time
jective measures. First, as shown in Table 4, Positive 2.28* .03
there were no relationships between peak pupil Negative 2.26* 2.00
Neutral 2.35** 2.02
dilation and current PANAS-C ratings. All 2.32* .00
Second, we examined whether peak pupil dila-
tion was associated with word recall and reaction Note: PANAS-C, Positive and Negative Affect
time. We conducted a repeated-measures regres- Schedule for Children (Laurent et al., 1999); Peak,
maximum dilation from 2 to 4 s; Late, average dilation
sion in which word recall was a repeated measure from 9 to 12 s.
and peak pupil dilation was a continuous explana- *p , .05.
tory variable. There was a significant peak
Pupil Dilation  Valence interaction for recall measure and peak pupil dilation was a continu-
for emotional versus neutral words, F (1, 64) ous explanatory variable. There was a signifi-
5.14, p , .05. To interpret this effect, we exam- cant main effect for peak pupil dilation that
ined correlations between pupil dilation and was not moderated by valence, F (1, 64)
word recall separately for emotional and neutral 7.05, p , .01. As shown in Table 4, greater in-
words. As shown in Table 4, overall peak pupil itial peak pupil dilation was associated with
dilation was associated with greater recall of emo- faster reaction times on the emotional word
tional words (r .31, p , .05), but was not asso- VID task regardless of word valence
ciated with recall of neutral words (r 2.08, ns). (rallvalences 2.32, p , .05).
Third, we conducted a repeated-measures re- We also examined whether late (912 s) pu-
gression in which reaction time was a repeated pil dilation to all words was associated with
Puberty and pupillary reactivity 19

behavioral or subjective ratings of emotional in- VID task with puberty was moderated by
formation processing. As shown in Table 4, late word valence. This parallels Quevedo et al.s
pupil dilation was not correlated with subjective (2008) finding of increased startle response
ratings of emotionality in the lab. Repeated- with puberty during an affective pictures para-
measures regressions indicated that late pupil digm irrespective of picture valence. Our find-
dilation was not associated with word recall or ing of increased puberty-linked pupillary reac-
reaction time, either alone or in interaction tivity on the emotional word identification
with word valence. task could have occurred through at least two
mechanisms: (a) increased devotion of general
cognitive processing resources in the pubertal
Discussion
group or (b) increased affective reactivity in
In this study, we found evidence that cognitive the pubertal group. Because pupil dilation pro-
and affective processes involved in classifying vides a summative index of task-related cog-
the emotionality of words appear to undergo nitive and affective brain activity (Siegle, Stein-
alterations during pubertal maturation. These hauer, Stenger, et al., 2003), and because we
cognitiveaffective changes were apparent in did not include a purely cognitive task in our
measures of psychophysiology, memory bias, protocol, we cannot rule out the possibility
and subjective ratings of emotion among that the increased pupillary reactivity is driven
children in the mid or late stages of puberty primarily by more cognitive processes, such
compared to children and adolescents who as reading and classifying the word. However,
were prepubertal or in the beginning stages of given that pubertal children and adolescents
puberty. First, mid-/late pubertal children and were generally older, it would be expected
adolescents showed greater peak pupillary reac- that these participants would have an easier
tivity to words during an emotional word iden- time performing the cognitive aspects of the
tification paradigm than pre-/early pubertal task. Thus, we would expect them to devote
children and adolescents. This peak pupil dila- less mental resources to cognitive aspects of
tion was associated with greater memory for the task such as reading and classifying words
emotional but not neutral words on an unex- than pre- and early pubertal children, resulting
pected free recall task, suggesting that it may in smaller mental effort-related pupil dilation
be linked to emotionally relevant processing. relative to pre- and early pubertal participants.
This finding was replicated controlling for par- In addition, we found that participants
ticipants age, and was not found using age ra- whose pupils initially dilated more in response
ther than puberty as a predictor, suggesting that to the words presented in the emotional valence
the effect is puberty specific. Second, mid-/late identification task remembered more emotional
pubertal children and adolescents showed a bias words in the unexpected recall task. Initial pupil
toward remembering more emotional words dilation was not associated with memory for
than pre-/early pubertal children on an unex- neutral words. This suggests that initial pupil
pected free recall task following the emotional dilation was related to emotional biases in
word identification paradigm. Third, we also word retrieval, an important late-stage compo-
found that mid-/late pubertal children rated nent of information processing models (e.g.,
themselves as higher in emotionality, especially Anderson, Qin, Jung, & Carter, 2007). This
negative affect, during their laboratory visit finding, in conjunction with the emotional con-
than pre-/early pubertal children. text of the task, in which participants attention
These results are generally consistent with was explicitly directed toward evaluating the
models suggesting that puberty is associated emotional qualities of the words presented, sug-
with greater reactivity of neurobehavioral sys- gest that the pubertal difference in peak pupil
tems involved in emotional information pro- dilation is at least partially driven by affective
cessing (Dahl, 2001; Nelson et al., 2005; Spear, processes.
2000; Steinberg, 2005; Steinberg et al., 2006). There may also be important maturational
However, we did not find that the increased in- changes in cognitive systems related to these
itial pupillary response on the emotional word findings, such as changes in reactivity to verbal
20 J. S. Silk et al.

stimuli or engagement in reading. Our use of maturation of the neural systems involved in
verbal stimuli is particularly relevant here. cognitiveemotional integration, particularly
Booth et al. (2001, 2004) have proposed that ce- the impact of puberty.
rebral maturation occurring after puberty could The lack of valence moderation in the pre-
lead to the automatization of reading routines. sent study appears to be explained by the fact
Specifically, they hypothesize that brain mat- that children in our sample had a strong pupil-
uration, along with increased practice and ex- lary reaction to neutral words as well as to emo-
posure, leads to specialization of a network of tional words. In fact, there was a trend for pupil
left brain regions involved in reading including dilation across the waveform to be greater
the angular or supramarginal gyrus. However, to neutral words than to emotional words, al-
the extent of changes in reading-related neural though it was not replicated across a long
activity beyond late childhood and the timing enough segment of the waveform to be consid-
of such changes relative to puberty is still ered significant. There are at least two potential
poorly understood (see Proverbio & Zani, explanations for this relatively strong pupillary
2005). Future research is also needed to exam- reactivity to neutral words. First, because par-
ine whether pubertal differences in pupil dila- ticipants attention was directed toward evaluat-
tion are found in more purely cognitive infor- ing the emotional aspects of each word, partic-
mation processing tasks, as well as affective ipants may have been more likely to view
tasks with both verbal and nonverbal stimuli. neutral words in an emotional context. Re-
Even more likely is the possibility that pu- search has shown that the interpretation of neu-
berty is linked with changes in processes that tral stimuli can vary depending on the valences
are at the interface of cognitive and emotional of the other stimuli presented during the exper-
processing. The valence identification task, imental context (Russell & Fehr, 1987). For ex-
which requires youth to make cognitive deci- ample, the word pen, when viewed alone,
sions about potentially emotional stimuli, is may appear relatively neutral; but when asked
an example of this type of integration. It re- to evaluate its emotionality an adolescent may
quires participants to cognitively process (i.e., begin to think about school and homework
pay attention to and classify words according and attach a negative evaluation to this word.
to valence) emotionally salient information. Al- In fact, we conducted debriefing interviews on
though tasks that require the integration of cog- a small number of subjects and were struck by
nitive and emotional functions need specific the idiosyncratic positive and negative qualities
methodological designs to be able to tease apart several youth attached to seemingly neutral
and draw firm conclusions about cognitive ver- words such as pen and sheep and tree.
sus affective systems, these types of tasks are It may be that there are few inherently neutral
representative of the types of processes impli- words. Consistent with this explanation, Siegle
cated in the decisions and dilemmas that adoles- et al. also found that unmedicated depressed
cents are faced with on a daily basis. These de- adults initial pupil dilation does not differ as
cisions rarely require pure cognitive processing a function of word valence when attention is di-
or pure emotional processing (they require an rected toward identifying emotional valence of
integration of the two), and this integration words (Siegle et al., 2001), although valence
may be the adolescents biggest challenge. specificity was observed in medicated de-
For example, Reyna and Farley (2006) reported pressed adults (Siegle, Steinhauser, Carter,
that although adolescents are capable of arriv- et al., 2003).
ing at the same judgments about risky decisions Second, stimuli that are novel and ambigu-
(e.g., drunk driving) as adults, they are some- ous can be arousing (Schwartz et al., 2003;
what slower in their response. Baird, Fugel- Whalen, 1998). For example, Schwartz et al.
sang, and Bennett (2005) demonstrated that (2003) have shown increased amygdala activity
such behavioral differences were related to dif- in novel versus familiar faces, all with a neutral
ferences in the neural circuitry recruited in ado- expression. This is theorized to occur because
lescents compared to adults. Future studies are the amygdala acts to detect and process un-
needed that are designed to explicitly test the expected or unfamiliar information that might
Puberty and pupillary reactivity 21

have potential biological importance (Schwartz indicate increased limbic reactivity or increased
et al., 2003; Whalen, 1998). Because neutral engagement of regulatory structures. The use of
words may be ambiguous in terms of their va- pupil dilation alone cannot distinguish between
lence, these words might elicit greater reactivity purely emotional reactions and other processes,
of neural systems. such as emotion regulation, that also involve
There is some evidence that youth in particu- cognitive components (Urry et al., 2006). This
lar may have a tendency to show affective reac- lack of specificity is a limitation to the pupil-
tions to neutral stimuli during experimental pro- lometry approach that could be addressed in
cedures. For example, Thomas et al. (2001) future research using concurrent collection of
found that children had greater amygdala reac- pupillometric and neuroimaging data, which
tivity to neutral faces than adults. Youth may is now available in many fMRI environments
thus be more sensitive to the ambiguity of neu- (see Siegle et al., 2003b).
tral stimuli, or, especially among pubertal chil- One of the strengths of this study is that we
dren, have a tendency to see emotion even in were able to show that increased pupil dilation
nonemotional stimuli. Reactivity to neutral to negative words was specific to the effects
stimuli based on either ambiguity or overgener- of puberty above and beyond participants
alization of emotion would likely be intensified age. Disentangling pubertal and age effects is
when children are asked to classify the valence an important but challenging task given that
of neutral words, a task that is much easier for the two are highly related. There is a need for
words that are obviously positive or negative future studies to be designed in ways that will
than for ambiguous neutral words. These find- facilitate the identification of puberty-specific
ings do, however, differ from our previous effects, such as selecting youth matched on
study, which included a small sample of 8- to age but differing on pubertal status (i.e., this is-
17-year-old typically developing children as sue, Quevedo et al., 2009). Using this approach,
well as children with MDD. In this study, we the researcher can attribute group differences to
found that childrens initial pupil dilation was pubertal effects without having to include a sta-
greater following negative words than neutral tistical covariate for age in the model. Obtain-
or positive words (Silk et al., 2007). Although ing the most precise measure of puberty that
both studies used the same words, there were is possible, such as Tanner staging via physical
a number of differences in the context in which examination, will also enhance researchers
the task was completed in the two studies, such ability to detect puberty-specific effects.
as time of day, distance from computer screen, We also found that sustained pupillary re-
and length of overall study (participants in the sponses among children in mid- to late puberty
MDD study stayed in the laboratory overnight). were smaller compared to children and adoles-
Future research with larger samples of both cents who were prepubertal or in the initial
typically developing and clinical populations stages of puberty. Mid-/late pubertal children
of children is needed to resolve this issue. and adolescents showed decreased pupil dila-
There are several potential brain mecha- tion to all words on average in the last second
nisms that might underlie this increased initial of the trial compared to pre-/early pubertal chil-
pupil dilation during the emotional word iden- dren and adolescents, regardless of word va-
tification task. Pupil dilation results from exten- lence. Unlike the peak pupil dilation response,
sive inputs from both cortical and limbic re- this sustained response was not related to mem-
gions of the brain mediated via sympathetic ory for emotional words or reaction time. We
and parasympathetic pathways (Steinhauer, have previously observed a more pronounced
Siegle, Condray, & Pless, 2004). Pupil dilation decrease in late pupil dilation response to below
has been associated with stimulation of the baseline levels in depressed children and ado-
amygdala (Koikegami & Yoshida, 1953) as lescents relative to controls that is specific to
well as stimulation of the frontal cortex and an- negative words and is correlated with other in-
terior cingulate cortex via connections from the dices of emotionality (Silk et al., 2007); how-
midbrain reticular formation (Beatty, 1986). ever, this difference among typically develop-
Thus, increased initial pupil dilation could ing children and adolescents is more subtle,
22 J. S. Silk et al.

occurs over a shorter region of the waveform, Finally, we relied on verbal affective stimuli.
and is less clearly associated with emotional We chose to use words because they are less
processes. The present finding might indicate visually complex and thus can be more easily
that children further along in puberty are disen- balanced for visual characteristics, such as lu-
gaging their attention from the task more than minosity, that can affect pupil dilation. Despite
pre- and early pubertal children when the this advantage, words are subject to develop-
word is no longer on the screen. These adoles- mental differences in reading speed and may
cents might be more bored, or might be demon- also be less ecologically valid than affective
strating improved skills in refocusing attention faces or pictures. However, affective words
away from emotional material relative to pre- have now been used successfully in several
and early pubertal children. Although studies studies with child and adolescent samples,
have investigated differences in attentional con- and have been useful in delineating develop-
trol between adolescents and adults (e.g., Monk mental pattern of emotional processing (Perez
et al., 2003), little is known about changes in at- Edgar, & Fox, 2003) as well as revealing altera-
tentional control as a function of puberty, and tions from normative patterns of emotional in-
further research is needed in this area. formation processing in studies youth with
Contrary to our hypotheses, we also found and at risk for mood disorders (Gotlib, Traill,
that mid-/late pubertal children and adolescents Montoya, Joormann, & Chang, 2005; Neshat-
had faster reaction times to all words than Doost, Taghavi, Moradi, Yule, & Dalgleish,
pre-/early pubertal children and adolescents. 1998; Silk et al., 2007) and anxious youth (Ta-
This finding may be a function of faster reading ghavi, Dalgleish, Moradi, Neshat Doost, &
speed among children further along in puberty, Yule, 2003; Vasey, El-Hag, & Daleiden, 1996).
as these children are also older. Nevertheless, This study also has several notable strengths.
faster reaction time was associated with remem- It utilized a multimethod approach including
bering more emotional words, suggesting that physiological, behavioral, and subjective mea-
faster reactions may be reflecting an attentional sures of emotional information processing
bias toward the emotional words. in conjunction with pubertal assessment, a
domain often overlooked in developmental
research. This is the first study of which we
Strengths and limitations
are aware to assess pupil dilation to emotional
Several limitations of the present study should stimuli in typically developing children and
be noted. The sample was small, limiting our adolescents. Findings suggest that this novel
power to detect small to moderate effects. The approach is a promising method for understand-
small sample also limited our ability to examine ing emotional information processing in chil-
gender by puberty interactions and to explore dren and adolescents. It provides strong tem-
differences between prepubertal and early pu- poral precision regarding the pattern of early
bertal children and between mid- and late and late emotional processing that is not
pubertal children. Reliance on child report to available by self-report or even by many other
assess puberty is another limitation; however, psychophysiological measurement approaches.
there is evidence that the PDS correlates with Furthermore, pupil dilation is measured using
Tanner Stages on physical exam and hormonal noninvasive and affordable techniques that
measures of puberty (Brooks-Gunn et al., 1987; were easily tolerated by children. Research
Shirtcliff et al., 2007). We also acknowledge with clinical samples of depressed adults
that the median split used to create pubertal sta- (Siegle et al., 2001; Siegle, Steinhauer, Carter,
tus groups is relatively arbitrary. As discussed et al., 2003) as well as our initial work with de-
above, future research would benefit from ob- pressed children (Silk et al., 2007) suggest that
taining measures of pubertal development pupil dilation to emotional words may have
(e.g., physical exam) that are more precise and clinical relevance, which is particularly exciting
thus can be included in analyses with age and because pupil dilation could eventually be mea-
can be used to create groupings that are less sured in clinical settings. The finding that the
arbitrary. pubertal differences in pupil dilation remained
Puberty and pupillary reactivity 23

significant controlling for age suggests that this ing throughout adolescence (Sowell & Jerni-
method may be indexing an important neurobe- gan, 1998), the pubertal window is a critical pe-
havioral change that is specific to pubertal riod for parents, teachers, and other adults to
maturation. Future concurrent pupil/fMRI stud- support children in practicing and refining skills
ies may be able to combine the temporal spec- for emotion regulation. Paradoxically, this oc-
ificity of the pupillometry approach with the curs at a time when parents may be inclined to
spatial specificity of the fMRI approach to de- distance themselves from their children emo-
lineate the specific neural systems underlying tionally. Despite more physically mature ap-
these puberty-linked changes in the time course pearances and more conflictual parentchild
of pupillary response to emotional words. relationships (Steinberg, 1987), parents remain
critical sources of support for adolescents dur-
ing the emotional journey through puberty
Clinical implications
(Steinberg & Silk, 2002). The pubertal period
The findings of the present study support mod- may also provide a window of opportunity for
els that view puberty as a period of enhanced intervening in clinical and vulnerable popula-
sensitivity to emotional stimuli (Dahl, 2001; tions of children. Early intervention during
Spear, 2000; Steinberg, 2005; Steinberg et al., this period of relative plasticity could lead to
2006). Given evidence that prefrontal systems long-term reductions in health-related cost and
subserving regulatory control are still develop- suffering in adulthood.

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