-
Title
-
The Neurobiology and Physiology of Emotions: A Developmental Perspective
-
Author
-
Kahle, Sarah S.
-
Hastings, Paul D.
-
Research Area
-
Cognition and Emotions
-
Topic
-
Emotional Development
-
Abstract
-
This essay discusses the physiological and neural activity associated with emotion processes, with a focus on the development of this activity in children. We review some conceptual issues about the distinctions between the components of emotion, including the physiology associated with emotions themselves, attempts to regulate emotions, and trait or state patterns of responding. Foundational work examining autonomic nervous system activity is summarized, and we highlight recent work that attempts to investigate emotion processes in multiple systems. We then suggest that two fruitful avenues of future research include the examination of the neurobiology and physiology of social emotions, and further investigation into the temporal dynamics of emotion processes.
-
Identifier
-
etrds0237
-
extracted text
-
The Neurobiology and Physiology
of Emotions: A Developmental
Perspective
SARAH S. KAHLE and PAUL D. HASTINGS
Abstract
This essay discusses the physiological and neural activity associated with emotion
processes, with a focus on the development of this activity in children. We review
some conceptual issues about the distinctions between the components of emotion,
including the physiology associated with emotions themselves, attempts to regulate
emotions, and trait or state patterns of responding. Foundational work examining
autonomic nervous system activity is summarized, and we highlight recent work
that attempts to investigate emotion processes in multiple systems. We then suggest
that two fruitful avenues of future research include the examination of the neurobiology and physiology of social emotions, and further investigation into the temporal
dynamics of emotion processes.
INTRODUCTION
Research on the neurobiology of emotional processes has largely proceeded
along two lines. Basic emotion perspectives drive the search for dedicated
circuits for specific and discrete emotions in the brain, body, and behavior,
whereas psychological constructionist perspectives seek shared underlying
components or dimensions of activity in the brain and body that come
together during the experience of many emotions. Common to these perspectives is the recognition that physiological activity is a critical component
of emotion and that examining physiology offers a deeper understanding
of emotion processes. Importantly, there appear to be typical responses of
the brain and body that are specific to, or differentiate between, certain
emotions, but also great individual variation in physiological responses to
emotions that have implications for regulation, behavior, and adjustment.
In our work, we have focused on examining the development of the physiological aspects of emotion (Hastings, Kahle, & Han, 2014). A developmental
Emerging Trends in the Social and Behavioral Sciences. Edited by Robert Scott and Stephen Kosslyn.
© 2015 John Wiley & Sons, Inc. ISBN 978-1-118-90077-2.
1
2
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
approach explicitly acknowledges that the etiology and ontology of adult
functioning cannot be fully understood without identifying the origins and
trajectories of emotions in childhood. In this chapter, we focus extensively on
the activity of the autonomic nervous system (ANS) and how it is associated
with two other core aspects of emotions and neurobiology: the brain and the
hypothalamic-pituitary-adrenocortical (HPA) axis. We highlight the importance of multimethod research designs that integrate activity across multiple
physiological systems, and we touch on some of the cutting-edge work in
this area. We then put forth two areas of future work that we think would
have exciting implications for our understanding of emotion in children—the
physiology of social emotions, such as guilt and pride, and the temporal
dynamics of emotion physiology. Throughout, we aim to provide greater
insight into of a few of the many interesting issues and exciting avenues of
work in the study of emotion, biology, and development.
DEFINING EMOTION
Functional and evolutionary theories of emotion posit that emotions are
biologically based processes that facilitate adaptation to changing conditions
(Campos, Mumme, Kermoian, & Campos, 1994; Cole, Martin, & Dennis,
2004). In response to an evocative situation, emotions ready the body to
respond in order to either maintain circumstances that are positive or change
those that are negative. Thus, emotions regulate thoughts, physiology, and
behavior. Yet, emotions themselves can also be targets of regulation. Emotion
regulation typically involves efforts to change the onset, duration, offset,
or intensity of the physical, cognitive, and behavioral components of an
emotion. How, and even whether, emotions are dissociable from emotion
regulation is an area of ongoing discussion (Cole et al., 2004; Thompson,
2011). In most of the work we describe here, the observed physiological
and neural responses to emotion likely partially reflect children’s attempts
at regulating emotion in addition to their experience and expression of
emotions themselves.
Another important distinction is that of trait versus state measures of emotion. Persistent moods or tendencies to feel certain emotions are distinct from
emotion experiences that are temporary or in-the-moment. Similarly, baseline measures of physiology more likely reflect trait-like levels of activity
in the brain and body, while measures of reactivity to an event or stimulus
reflect a more specific, contextually-bound response. For example, we would
expect a tendency to feel fear and anxiety to be reflected in a baseline measure of physiology, such as high resting heart rate. A transient fear experience
would more likely relate to reactive physiology, such as an increase in heart
rate. We discuss research addressing both of these issues.
The Neurobiology and Physiology of Emotions: A Developmental Perspective
3
An exciting problem for developmentalists is that all of these components
undergo change during childhood. Physiological systems change with
experience and maturity, meaning that even trait-like baseline measures can
look different over time. Children increasingly experience more varied and
nuanced emotions and become able to implement more sophisticated forms
of emotion regulation. We next summarize classic and cutting-edge research
that addresses these complicated developmental issues.
FOUNDATIONAL RESEARCH
AUTONOMIC NERVOUS SYSTEM
As the longest studied and arguably most well-understood aspect of emotion
physiology, there is a rich history of work on the ANS. It is also a critical system for the functional aspects of emotion in that it prepares the organs and
muscles of the body to act in accord with an emotion (e.g., releasing glucose
in order to run in response to fear). The ANS is the bidirectional connection
between brain and body, and while we argue later that studying both systems
is important to capture this communication, examining the ANS provides an
indirect way of studying central processing. We first summarize some foundational research using heart rate as an index of autonomic activity before
discussing more recent attempts to parse the activity of the two autonomic
branches from other cardiac measures.
Early work by Joseph Campos tended to conclude that in infants, heart
rate deceleration was indicative of interest or attention, while heart rate
acceleration was associated with fear or wariness, or negative affect more
generally (e.g., Campos, Emde, Gaensbauer, & Henderson, 1975). In a
handful of studies, sadness has been fairly consistently linked with slower
heart rate in children, while anger and fear have been related to faster heart
rate (e.g., Eisenberg et al., 1988; Lewis, Ramsay, & Sullivan, 2006). Other
researchers have interpreted heart rate acceleration as general arousal, which
could be negatively or positively valenced (Field, 1982). The interpretation
of changes in heart rate continues to be debated (Obradovi´c & Boyce, 2012).
Developmental changes in emotion processes may be one reason for the
lack of clear associations between physiology and distinct emotions. Work
by Campos and colleagues showed that autonomic responses to the same
stimulus can change over time. As infants gained experience with crawling
and heights, they began to show heart rate acceleration to a visual cliff,
suggesting a fear response, while younger infants tended to show heart rate
deceleration, indicative of interest (Schwartz, Campos, & Baisel, 1973).
Multiple factors determine heart rate, which may be another reason for
inconsistencies. The parasympathetic nervous system (PNS) is generally
4
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
associated with restorative actions (e.g., digestion, sleep) while the sympathetic nervous system (SNS) generally prepares the body for activity
(e.g., fight or flight behaviors), and both are associated with emotion.
These opposing effects initially led researchers to consider the activity of
the two branches as antagonistic; however, further work showed that the
SNS and PNS interact in complex ways, including being coactivated or
coinhibited (Berntson, Cacioppo, Quigley, & Fabro, 1994). Heart rate reflects
the activity of both branches, but certain aspects of the cardiac cycle have
been specifically attributed to PNS or SNS influence. Respiratory sinus
arrhythmia (RSA) is a measure of heart rate variability that is controlled by
the vagus nerve, which reflects PNS influence. Higher RSA means greater
PNS influence. Preejection period (PEP) indexes heart contractility, the
elapsed time between depolarization of the left ventricle and the opening of
the aortic valve, which is under SNS control. Shorter (i.e., faster) PEP means
more SNS influence.
Developmental work examining the specific role of the PNS in responding
to social and emotional stimuli has been based considerably on Porges’
polyvagal theory (1995, 2007). Because the vagus nerve, the primary efferent
of the PNS, tonically downregulates cardiac activity, decreases in vagal
influence can increase heart rate without mounting a sympathetic response,
which has high metabolic costs. Research has generally shown that high
baseline parasympathetic influence is related to more adaptive patterns
of emotion expression and regulation (Beauchaine, 2001). However, what
constitutes “adaptive” may change over development. An influential
study by Porges and colleagues (1994) showed that at 9 months, greater
parasympathetic influence was positively correlated with concurrent
maternal ratings of difficult temperament, but predicted lower ratings of
difficult temperament at 3 years. Early difficult behaviors might elicit parent
responses that effectively support the child’s attaining better regulation
of emotion. Alternatively, the links between the PNS and emotion might
undergo fundamental changes in early childhood.
A large body of work has also examined reactive change in parasympathetic activity during emotion. Emotion inductions tend to produce
a decrease in PNS influence, or increases in arousal, but comparisons
across different emotions in children are rare. In adults, anger and fear
are associated with decreases in PNS influence, while sadness tends to be
associated with parasympathetic activation. Positive emotions are often
also linked with parasympathetic activation, although findings are more
mixed (Kreibig, 2010). In general, a modest withdrawal of parasympathetic
influence in response to social, emotional, or cognitive challenges tends
to reflect self-regulation and positive functioning in children (Beauchaine,
2001; Blair & Peters, 2003; Marcovitch et al., 2010). However, in line with
The Neurobiology and Physiology of Emotions: A Developmental Perspective
5
the polyvagal theory, maintaining high parasympathetic influence has been
shown to support positive social engagement (Hastings & Miller, 2014;
Hastings et al., 2008).
The SNS is also sensitive to emotion. While RSA is the only noninvasive
index of PNS activity, SNS activity can be measured several ways in addition
to PEP. The SNS controls sweat gland activity, so skin conductance levels
(baseline) or responses (reactivity) proxy SNS activity. Levels of the enzyme
alpha amylase in saliva have also been linked to SNS activity. In children,
having higher resting levels of sympathetic influence has been related to
showing fearful behaviors, even in very mildly threatening circumstances
(Buss, Davidson, Kalin, & Goldsmith, 2004). Fear and anger have been associated with increases in sympathetic activity reflected in shortening PEP or
increases in skin conductance in children and adults (Baker, Baibazarova,
Ktistaki, Shelton, & Van Goozen, 2012; Kreibig, 2010). Interestingly, research
with adults also has distinguished between different aspects of positive emotional states. For example, happiness has been associated with increased SNS
activity, but contentment with decreased (Kreibig, 2010). A parallel distinction has not been made in studies of children to our knowledge.
Recently, researchers have begun to look at the joint contributions of
both autonomic branches by examining children’s profiles of autonomic
activity. Maturational changes lead to higher RSA and longer PEP at
baseline, reflecting a resting state that becomes more parasympathetically
dominated (Alkon, Boyce, Davis, & Eskenazi, 2011; Hinnant, Elmore-Staton,
& El-Sheikh, 2011). There is some evidence for an analogous shift in reactive
ANS activity as well (Alkon et al., 2003), but more work is needed to confirm
this finding. Profiles of autonomic activity also vary depending on the
emotional context. In one study, a reaction time task produced profiles that
involved sympathetic activation (and either parasympathetic activation or
withdrawal), while a social interview produced patterns of parasympathetic
withdrawal (and either sympathetic activation or withdrawal; Salomon,
Matthews, & Allen, 2000). Some progress has thus been made in integrating
the activity of the two branches of the ANS. However, the rest of the body’s
systems are similarly interconnected (Berntson & Cacioppo, 2007). Next, we
discuss work that is beginning to examine these connections across multiple
systems.
CUTTING-EDGE RESEARCH
MULTIPLE LEVELS OF ANALYSIS
Research on the physiology of stress overlaps with emotion research, and
one reason why these constructs are connected is because the systems that
6
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
respond to stress and emotion intersect. One key stress-response system in
the body is the HPA axis, which has as one of its primary outputs, cortisol,
a neuroendocrine hormone that is easily measured via salivary secretions.
Cross-talk among the brain and the autonomic and endocrine systems is critical to coherent and appropriate responses to emotions. Some brain structures
appear to be especially involved in this integration of emotion information
across systems, such as the anterior cingulate cortex and the hypothalamus
(Berntson & Cacioppo, 2007; Dennis, 2010).
Some research has examined emotion processes across systems. In two
studies, ANS activity was associated with young children’s approach
behaviors and emotions—both happiness and anger—while cortisol was
associated with withdrawal emotions—fear and sadness (Fortunato, Dribin,
Granger, & Buss, 2008; Lewis et al., 2006). These systems show selective
responses to stimuli, with the ANS priming the body to engage and act
and the HPA axis promoting withdrawal. This also suggests that emotions
associated with withdrawal behaviors (e.g., sadness) may produce more of a
stress response than other emotions. This kind of specificity in emotion may
facilitate targeted actions, thoughts, and behaviors to the situation at hand.
One reason why this line of research has not advanced further may be the
dearth of theoretical models for how and when multiple systems coordinate. Miskovic and Schmidt (2012) have recently drawn on classic principles
of approach/avoidance behavior to put forth a theoretical framework for
brain–body interactions. They argue that the brain hemispheres, as well as
autonomic inputs and outputs, are lateralized, such that the right side is associated with energy-consuming activities (SNS-driven cardiac acceleration,
cortisol secretion), while the left side is associated with energy-replenishing
activities (PNS-driven cardiac deceleration, inhibition of the amygdala). In
support, they showed that fearful children had greater right frontal brain
activity (as measured by electroencelophography; EEG), higher heart rate,
and increased SNS and amygdala activity.
The notion that the brain and body encompass multiple, dynamically
interacting systems may seem obvious, but the measurement, analysis, and
interpretation of integrative physiology is extremely complex. Given that the
connections between these systems—and the systems themselves—develop
and change across childhood, much more theoretical and empirical work
is needed to establish normative and aberrant patterns of physiological
responses that correspond with emotion processes across development.
FUTURE DIRECTIONS
Next, we highlight two directions for future work that would contribute to
our understanding of the physiology of children’s emotions. First, we suggest
The Neurobiology and Physiology of Emotions: A Developmental Perspective
7
a greater focus on the biology of social emotions, which have been underinvestigated in both children and in adults. Second, we recommend a closer
look at the temporal dynamics of emotion physiology, particularly the termination of emotion responses and the return or recovery to baseline.
SOCIAL EMOTIONS
With the exception of empathy (Hastings, Miller, Kahle, & Zahn-Waxler,
2014), the biological correlates of social emotions have received less attention
than those of basic emotions, particularly in the developmental literature.
Emotions such as guilt, shame, pride, embarrassment, and empathy are
termed “social” because some understanding of others’ minds is required.
For example, in order to feel guilt, one needs to understand that they have
caused some harm or disappointment to someone else. These emotions are
also social in that they serve to promote social norms and rules.
Brain areas that are associated with social emotions are also implicated in
other processes related to understanding the self and others, such as theory of
mind, and broadly include the amygdala and areas of the frontal and temporal lobes (for a review, see Beer, 2007). One study has compared brain activity
to embarrassment and guilt (vs basic emotions) in adolescents and adults
(Burnett, Bird, Moll, Frith, & Blakemore, 2009). Both groups showed activity
in the anterior rostral area of the medial prefrontal cortex (mPFC); but adolescents showed more lateral anterior rostral mPFC activation, whereas adults
showed more left temporal activation. The suggestion that regions associated with these emotions change with development mirrors aspects of B.J.
Casey’s work (Casey, Jones, & Hare, 2008) showing that differential trajectories of brain maturation influence adolescents’ impulsive decision making. It
will be important for developmental affective neuroscientists to identify the
functional or behavioral effects of these differences.
Embarrassment and shame have been associated with cortisol and protracted arousal in preschoolers (Lewis & Ramsay, 2002; Mills, Imm, Walling,
& Weiler, 2008). Interestingly, Lewis and Ramsay (2002) found that this was
only true for embarrassment that was in response to failure. Decreases in
cortisol were associated with preschoolers showing embarrassment due to
their success. This shows distinct associations between emotions and physiology that are context dependent, and is another instance of specificity in
physiological responses.
Baker and colleagues (2012) found an interesting developmental association between fearlessness and guilt: behavioral and physiological indicators
of fearlessness (low heart rate and SCL) in infancy predicted low physiological arousal during a guilt paradigm in toddlerhood. In order to feel guilt, one
needs to understand that one’s actions caused someone else to feel bad, an
8
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
insight that infants may not be yet capable of. Yet, physiological signals to
fear, which are present early in development and alert the infant to potential
threats in the environment, may support the future interpretation of physiological responses to their own wrongdoing as threats to their social self.
How earlier physiological responses to basic emotions may lay the foundation for later, more complex emotion experiences is an interesting question
for future work.
Just as positive emotions, such as joy and contentment, have received less
empirical attention than negative emotions, there have been fewer studies
of the physiology of pride than of embarrassment, guilt, or shame. In a few
adult studies, pride has been associated with increases in skin conductance,
but little or no change in many other measures (Kreibig, 2010). Lewis and
Ramsay (2002) found cortisol to be unrelated to pride in children, but further examinations of systems that are more likely to be active in response to
positive emotions are needed in children.
TEMPORAL DYNAMICS
The experience and expression of emotion are processes that unfold over
time. Thus, the physiological and neurological activity that accompanies
emotion experience and regulation is dynamic; the systems that become
active and the intensity of their activity varies over time (Fox, Kirwan, &
Reeb-Sutherland, 2012). However, the use of repeated physiological measurements to capture these patterns (vs levels) of change are rare, perhaps
due to the challenges involved in the measurement and analysis of dynamic
change. Statistical methods that estimate latent variables—such as latent
growth curve (LGC) models—are preferred for examining dynamic change
because they account for measurement error and handle missing data
(Bollen & Curran, 2006; Burt & Obradovic, 2013; Ram & Grimm, 2009). A
few studies have moved beyond the use of simple change scores to examine
patterns of change. Brooker and Buss (2010) provide one notable example.
They found that highly temperamentally fearful 2-year-olds showed a
pattern of increases followed by decreases in parasympathetic activity (as
measured by RSA) when they were approached by a stranger (a somewhat
frightening event for a toddler), whereas children low in temperamental fear
showed stable levels of parasympathetic activity. However, fearful children
who showed the dynamic pattern more strongly also showed greater
positive affect, suggesting that this was a supportive physiological response
for these fearful children. Examining the chronology of parasympathetic
influence revealed that children with different temperaments might also
utilize different regulatory mechanisms to achieve behaviorally similar
responses to emotional challenges.
The Neurobiology and Physiology of Emotions: A Developmental Perspective
9
Recent work in our laboratory used LGC modeling to track RSA changes in
4- to 6-year-olds during a video clip of an angry vignette (Miller et al., 2013).
RSA decreased (i.e., parasympathetic withdrawal) when the anger theme
was introduced, suggesting an orienting response, and then RSA increased as
anger intensified in the video, suggesting a regulatory or calming response to
the escalating emotion. Greater change in both directions was associated with
better regulation of aggression, showing that more dynamic RSA change over
the course of an anger episode is indicative of better parasympathetic regulation of anger.
Examinations of the dynamics of brain activity are gaining prominence,
but thus far have been pursued primarily with adults. For example,
Immordino-Yang and colleagues (2009) showed that feeling compassion for
physical pain was associated with an earlier peak and faster extinction of
activity in the anterior insula than for other social emotions. Thus, specificity
in the physiological concomitants of emotions can be seen both in terms of
which systems become active as well as the timing of this activity.
THE TERMINATION OF EMOTION: PHYSIOLOGICAL
AND NEUROLOGICAL RECOVERY
Researchers are beginning to touch on one aspect of the time course of emotion that we think is particularly important but relatively understudied—the
termination of the emotion and return to baseline. While physiological reactivity prepares the body to act in accord with an emotion, prolonged activation may inhibit adaptive behavior and flexible responding to ongoing
events. Adult studies have begun to show that autonomic recovery from
negative emotion is indeed distinct from reactivity, and is independently
associated with variables such as social isolation, poor mental health, hostility, and high negative affect (Llabre, Spitzer, Siegel, Saab, & Schneiderman,
2004; Steptoe & Marmot, 2006; Zellars, Meurs, Perrewe, Kacmar, & Rossi,
2009). Similarly, delayed recovery in amygdala responses to negative images
relates to higher levels of neuroticism (Schuyler et al., 2012).
Only a handful of studies have examined recovery processes in children,
and some links have been found with emotion regulation (Santucci et al.,
2008; Willeman, Schuengel, & Koot, 2009). We recently examined patterns
of sympathetic and parasympathetic activity in 3 1∕2-year-olds during a
frustration induction and a post-task recovery period (Kahle, Lopez, Miller,
& Hastings, 2013). During the task, sympathetic activity increased (shorter
PEP) while parasympathetic activity decreased (lower RSA), meaning
that both branches were working reciprocally to upregulate activity. After
the task, sympathetic activity began to decrease but parasympathetic
withdrawal continued, a pattern called coinhibition, indicating that the
10
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
branches were working in opposition. Only children’s sympathetic recovery
from frustration was associated with their mother’s reports of adjustment.
Children who showed greater sympathetic recovery (longer PEP in the
post-task period) had higher levels of emotion regulation and effortful
control. These relations suggest that while it is perhaps appropriate to show
physiological activation to frustration, the ability to quickly shut off the
sympathetic response once the situation improves is an adaptive response.
This is also another example of a system-specific response. Only sympathetic
activity during anger was related to regulation. While Miller and colleagues
(2013) found meaningful relations between PNS activity and regulation
in response to observing an angry interaction, this study found that SNS
activity in response to the experience of anger and frustration was related
to regulation. More work is needed to further investigate such possible
contextual effects on the physiology of emotion.
CONCLUSION
To describe one’s racing heart or cold sweat in response to emotion is
simple, but the scientific examination of these physiological phenomena
is less so. Our synthesis of the careful work done thus far shows that
we have learned quite a bit about emotions in the developing brain and
body, but it has also been revealed how much we still need to learn. For
example, one theme that emerged across studies is that some systems
respond in specific ways to some emotions some of the time. Difficult
questions about these aspects of context, timing, and multisystem involvement remain to be answered. Happily, in addition to gaining knowledge
about these processes, we have seen important developments in the tools
that might answer some of these tricky questions, such as multimethod,
longitudinal designs, and dynamic analysis approaches. Further elucidation of the developmental aspects of the neurobiology and physiology
of emotion will have important implications for our understanding of
emotion. To answer questions about why people act and feel the way they
do, we must look to the roots of emotional experience and responding in
childhood.
ACKNOWLEDGMENTS
This material is based on work supported by the National Science Foundation Graduate Research Fellowship under Grant No. 0707429.
The Neurobiology and Physiology of Emotions: A Developmental Perspective
11
REFERENCES
Alkon, A., Boyce, W. T., Davis, N. V., & Eskenazi, B. (2011). Developmental changes
in autonomic nervous system resting and reactivity measures in Latino children
from 6 to 60 months of age. Journal of Developmental and Behavioral Pediatrics, 32(9),
668–677. doi:10.1097/DBP.0b013e3182331fa6
Alkon, A., Goldstein, L. H., Smider, N., Essex, M. J., Kupfer, D. J., & Boyce,
W. T. (2003). Developmental and contextual influences on autonomic reactivity in young children. Developmental Psychobiology, 42(1), 64–78. doi:10.1002/
dev.10082
Baker, E., Baibazarova, E., Ktistaki, G., Shelton, K. H., & Van Goozen, S. H. M.
(2012). Development of fear and guilt in young children: Stability over time and
relations with psychopathology. Development and Psychopathology, 24(3), 833–845.
doi:10.1017/S0954579412000399
Beauchaine, T. P. (2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in
psychopathology. Development and Psychopathology, 13(02), 183–214. doi:10.1017/
S0954579401002012
Beer, J. S. (2007). Neural systems for self-conscious emotions and their underlying
appraisals. In J. L. Tracy, R. W. Robins & J. P. Tangney (Eds.), The self-conscious
emotions: Theory and research (pp. 53–67). New York, NY: Guilford Press.
Berntson, G., & Cacioppo, J. (2007). Integrative physiology: Homeostasis, allostasis,
and the orchestration of systemic physiology. In J. T. Cacioppo, L. G. Tassinary
& G. G. Berntson (Eds.), Handbook of psychophysiology (3rd ed., pp. 453–481). New
York, NY: Cambridge University Press.
Berntson, G. G., Cacioppo, J. T., Quigley, K. S., & Fabro, V. T. (1994). Autonomic space
and psychophysiological response. Psychophysiology, 31(1), 44–61. doi:10.1111/
j.1469-8986.1994.tb01024.x
Blair, C., & Peters, R. (2003). Physiological and neurocognitive correlates of adaptive
behavior in preschool among children in Head Start. Developmental Neuropsychology, 24(1), 479–497. doi:10.1207/S15326942DN2401
Bollen, K. A., & Curran, P. J. (2006). Latent curve models: A structural equation approach.
New Jersey, NJ: John Wiley & Sons.
Brooker, R. J., & Buss, K. A. (2010). Dynamic measures of RSA predict distress and
regulation in toddlers. Developmental Psychobiology, 52(4), 372–382. doi:10.1002/
dev.20432
Burnett, S., Bird, G., Moll, J., Frith, C., & Blakemore, S.-J. (2009). Development during
adolescence of the neural processing of social emotion. Journal of Cognitive Neuroscience, 21(9), 1736–1750. doi:10.1162/jocn.2009.21121
Burt, K. B., & Obradovi´c, J. (2013). The construct of psychophysiological reactivity: Statistical and psychometric issues. Developmental Review, 33(1), 29–57.
doi:10.1016/j.dr.2012.10.002
Buss, K. A., Davidson, R. J., Kalin, N. H., & Goldsmith, H. H. (2004). Context-specific
freezing and associated physiological reactivity as a dysregulated fear response.
Developmental Psychology, 40(4), 583–594. doi:10.1037/0012-1649.40.4.583
12
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
Campos, J., Emde, R. N., Gaensbauer, T. J., & Henderson, C. (1975). Cardiac and
behavioral interrelationships in the reactions of infants to strangers. Developmental
Psychology, 11(5), 589–601.
Campos, J., Mumme, D. L., Kermoian, R., & Campos, R. G. (1994). A functionalist
perspective on the nature of emotion. Monographs of the society for research in child
development, 59, 284–303.
Casey, B. J., Jones, R. M., & Hare, T. A. (2008). The adolescent brain. Annals of the New
York Academy of Sciences, 1124, 111–126.
Cole, P. M., Martin, S. E., & Dennis, T. A. (2004). Emotion regulation as a scientific construct: methodological challenges and directions for child development research.
Child Development, 75(2), 317–333. doi:10.1111/j.1467-8624.2004.00673.x
Dennis, T. A. (2010). Neurophysiological markers for child emotion regulation from the perspective of emotion-cognition integration: Current directions and future challenges. Developmental Neuropsychology, 35(2), 212–230.
doi:10.1080/87565640903526579
Eisenberg, N., Fabes, R. A., Bustamante, D., Mathy, R. M., Miller, P. A., & Lindholm,
E. (1988). Differentiation of vicariously induced emotional reactions in children.
Developmental Psychology, 24(2), 237–246. doi:10.1037/0012-1649.24.2.237
Field, T. (1982). Affective displays of high-risk infants during early interactions. In T.
Field & A. Fogel (Eds.), Emotion and early interaction (pp. 101–125). Hillsdale, NJ:
Lawrence Earlbaum Associates Inc. Publishers.
Fortunato, C. K., Dribin, A. E., Granger, D. A., & Buss, K. A. (2008). Salivary
alpha-amylase and cortisol in toddlers: Differential relations to affective behavior.
Developmental Psychobiology, 50(8), 807–818. doi:10.1002/dev.20326
Fox, N. A., Kirwan, M., & Reeb-Sutherland, B. (2012). Measuring the physiology of
emotion and emotion regulation – Timing is everything. Monographs of the Society
for Research in Child Development, 77, 98–108.
Hastings, P. D., & Miller, J. G. (2014). Autonomic regulation, polyvagal theory, and
children’s prosocial development. In L. Padilla-Walker & G. Carlo (Eds.), Prosocial development: A multidimensional approach (pp. 112–127). New York, NY: Oxford
University Press.
Hastings, P. D., Kahle, S., & Han, G. H.-P. (2014). Developmental affective psychophysiology: Using physiology to inform our understanding of emotional
development. In K. H. Lagattuta (Ed.) Children and Emotion. New Insights into
Developmental Affective Sciences Vol 26, pp 13–28. Basel, Switzerland, Karger,
(DOI:10.1159/000354347).
Hastings, P. D., Miller, J. G., Kahle, S., & Zahn-Waxler, C. (2014). The neurobiological
basis of empathic concern for others. In M. Killen & J. Smetana (Eds.), Handbook of
moral development (2nd ed., pp. 411–434). New York, NY: Psychology Press.
Hastings, P. D., Nuselovici, J. N., Utendale, W. T., Coutya, J., McShane, K. E., & Sullivan, C. (2008). Applying the polyvagal theory to children’s emotion regulation:
Social context, socialization, and adjustment. Biological Psychology, 79(3), 299–306.
Hinnant, J. B., Elmore-Staton, L., & El-Sheikh, M. (2011). Developmental trajectories
of respiratory sinus arrhythmia and preejection period in middle childhood. Developmental Psychobiology, 53(1), 59–68. doi:10.1002/dev.20487
The Neurobiology and Physiology of Emotions: A Developmental Perspective
13
Immordino-Yang, M. H., McColl, A., Damasio, H., & Damasio, A. (2009). Neural correlates of admiration and compassion. Proceedings of the National
Academy of Sciences of the United States of America, 106(19), 8021–8026.
doi:10.1073/pnas.0810363106
Kahle, S., Lopez, M., Miller, J., Hastings, P.D. (April, 2013). The role of autonomic recovery in the development of emotion regulation. Paper presented at the biannual meeting
of the Society for Research in Child Development, Seattle, WA.
Kreibig, S. D. (2010). Autonomic nervous system activity in emotion: A review. Biological Psychology, 84(3), 394–421. doi:10.1016/j.biopsycho.2010.03.010
Llabre, M. M., Spitzer, S., Siegel, S., Saab, P. G., & Schneiderman, N. (2004). Applying latent growth curve modeling to the investigation of individual differences in
cardiovascular recovery from stress. Psychosomatic Medicine, 66(1), 29–41.
Lewis, M., & Ramsay, D. (2002). Cortisol response to embarrassment and shame.
Child Development, 73(4), 1034–1045.
Lewis, M., Ramsay, D., & Sullivan, M. W. (2006). The relation of ANS and HPA
activation to infant anger and sadness response to goal blockage. Developmental
Psychobiology, 48, 397–405. doi:10.1002/dev.20151
Marcovitch, S., Leigh, J., Calkins, S. D., Leerks, E. M., O’Brien, M., & Blankson, A. N.
(2010). Moderate vagal withdrawal in 3.5-year-old children is associated with optimal performance on executive function tasks. Developmental Psychobiology, 52(6),
603–608. doi:10.1002/dev.20462
Miller, J. G., Chocol, C., Nuselovici, J. N., Utendale, W. T., Simard, M., & Hastings, P.
D. (2013). Children’s dynamic RSA change during anger and its relations with
parenting, temperament, and control of aggression. Biological Psychology, 92(2),
417–425. doi:10.1016/j.biopsycho.2012.12.005
Mills, R. S. L., Imm, G. P., Walling, B. R., & Weiler, H. A. (2008). Cortisol reactivity and
regulation associated with shame responding in early childhood. Developmental
Psychology, 44(5), 1369–1380. doi:10.1037/a0013150
Miskovic, V., & Schmidt, L. A. (2012). New directions in the study of individual differences in temperament: A brain-body approach to understanding fearful and
fearless children. Monographs of the Society for Research in Child Development, 77(2),
28–38.
Obradovi´c, J., & Boyce, W. T. (2012). Developmental psychophysiology of emotion
processes. Monographs of the Society for Research in Child Development, 77, 120–128.
Porges, S. W. (1995). Orienting in a defensive world: Mammalian modifications of
our evolutionary heritage. A polyvagal theory. Psychophysiology, 32(4), 301–318.
Porges, S. W. (2007). The Polyvagal Perspective. Biological Psychology, 74(2), 116–143.
doi:10.1016/j.bbi.2008.05.010
Porges, S. W., Doussard-Roosevelt, J. A., Portales, A. L., & Suess, P. E. (1994). Cardiac vagal tone: Stability and relation to difficultness in infants and 3-year-olds.
Developmental Psychobiology, 27(5), 289–300. doi:10.1002/dev.420270504
Ram, N., & Grimm, K. J. (2009). Growth mixture modeling: A method for identifying
differences in longitudinal change among unobserved groups. International Journal
of Behavioral Development, 33, 565–576. doi:10.1177/0165025409343765
14
EMERGING TRENDS IN THE SOCIAL AND BEHAVIORAL SCIENCES
Salomon, K., Matthews, K. A., & Allen, M. T. (2000). Patterns of sympathetic and
parasympathetic reactivity in a sample of children and adolescents. Psychophysiology, 37(6), 842–849.
Santucci, A. K., Silk, J. S., Shaw, D. S., Gentzler, A., Fox, N. A., & Kovacs, M.
(2008). Vagal tone and temperament as predictors of emotion regulation strategies in young children. Developmental Psychobiology, 50(3), 205–216. doi:10.1002/
dev.20283
Schuyler, B. S., Kral, T. R. A., Jacquart, J., Burghy, C. A., Weng, H. Y., Perlman, D. M.
… Davidson, R. J. (2012). Temporal dynamics of emotional responding: Amygdala
recovery predicts emotional traits. Social Cognitive and Affective Neuroscience, 1–6.
10.1093/scan/nss131
Schwartz, A. N., Campos, J. J., & Baisel, E. J. (1973). The visual cliff: Cardiac and
behavioral responses on the deep and shallow sides at five and nine months of
age. Journal of Experimental Child Psychology, 15, 86–99.
Steptoe, A., & Marmot, M. (2006). Psychosocial, hemostatic, and inflammatory correlates of delayed poststress blood pressure recovery. Psychosomatic Medicine,
531–537. doi:10.1097/01.psy.0000227751.82103.65
Thompson, R. A. (2011). Emotion and emotion regulation: Two sides of the developing coin. Emotion Review, 3(1), 53–61. doi:10.1177/1754073910380969
Willemen, A. M., Schuengel, C., & Koot, H. M. (2009). Physiological regulation
of stress in referred adolescents: The role of the parent-adolescent relationship.
Journal of Child Psychology and Psychiatry, and Allied Disciplines, 50(4), 482–490.
doi:10.1111/j.1469-7610.2008.01982.x
Zellars, K. L., Meurs, J. A., Perrewé, P. L., Kacmar, C. J., & Rossi, A. M. (2009). Reacting
to and recovering from a stressful situation: The negative affectivity-physiological
arousal relationship. Journal of Occupational Health Psychology, 14(1), 11–22.
doi:10.1037/a0013823
SARAH S. KAHLE SHORT BIOGRAPHY
Sarah S. Kahle, MEd, is a graduate student in developmental psychology at
the University of California, Davis, studying with Dr. Paul Hastings. After
completing her MEd in Mind, Brain, and Education at Harvard University,
she became interested in the development of self-regulation and emotion
in children. She is currently examining these topics from several angles,
including the investigation of individual differences in physiological patterns underlying regulatory processes and how parenting and physiology
support forms of self-regulation such as executive function.
PAUL D. HASTINGS SHORT BIOGRAPHY
Paul D. Hastings, PhD, is a professor of psychology and chair of the Psychology department at the University of California, Davis. His research interests
The Neurobiology and Physiology of Emotions: A Developmental Perspective
15
center around understanding the ways in which biological and environmental factors shape the trajectories of children’s emotional and social development, encompassing both normal and adaptive development as well as
atypical and maladaptive development.
Webpage: http://psychology.ucdavis.edu/Labs/Hastings
RELATED ESSAYS
Group Identity and Political Cohesion (Political Science), Leonie Huddy
Cultural Neuroscience: Connecting Culture, Brain, and Genes (Psychology),
Shinobu Kitayama and Sarah Huff
Emotion and Intergroup Relations (Psychology), Diane M. Mackie et al.
Regulation of Emotions Under Stress (Psychology), Amanda J. Shallcross et al.
The Intrinsic Dynamics of Development (Psychology), Paul van Geert and
Marijn van Dijk
Emotion Regulation (Psychology), Paree Zarolia et al.