Brain and Cognition 52 (2003) 79–87
www.elsevier.com/locate/b&c
Central and autonomic nervous system integration in emotion
Dirk Hagemann,a,b,* Shari R. Waldstein,b,c and Julian F. Thayera
a
c
Laboratory of Personality and Cognition, National Institute on Aging, National Institutes of Health, Gerontology Research Center,
5600 Nathan Shock Drive, Baltimore, MD 21224, USA
b
Department of Psychology, University of Maryland, Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21250, USA
Division of Gerontology, Department of Medicine, University of Maryland School of Medicine and Geriatrics Research Education and Clinical Center,
Baltimore Veterans Affairs Medical Center, 22 South Greene Street, Baltimore, MD 21201, USA
Accepted 26 September 2002
Abstract
Emotions involve physiological responses that are regulated by the brain. The present paper reviews the empirical literature on
central nervous system (CNS) and autonomic nervous system (ANS) concomitants of emotional states, with a focus on studies that
simultaneously assessed CNS and ANS activity. The reviewed data support two primary conclusions: (1) numerous cortical and
subcortical regions show co-occurring activity with ANS responses in emotion, and (2) there may be reversed asymmetries on
cortical and subcortical levels with respect to CNS/ANS interrelations. These observations are interpreted in terms of a model of
neurovisceral integration in emotion, and directions for future research are presented.
Ó 2003 Elsevier Science (USA). All rights reserved.
Keywords: Autonomic nervous system; Central nervous system; Dynamical models; Emotion; Hemispheric lateralization; Inhibitory control
1. Introduction
Emotions involve a complex mix of cognitive, affective, behavioral, and physiological responses (e.g., Bir€ hman, 1993; Oatley & Jenkins, 1996). At a
baumer & O
physiological level of analysis, much current research in
affective neuroscience seeks to elucidate the neural networks that underlie emotion. In this regard, results of
numerous investigations of the central nervous system
(CNS) concomitants of emotion suggest the involvement
of multiple cortical (e.g., frontal, temporal, and parietal)
and subcortical (e.g., basal ganglia, thalamus, amygdala,
and hippocampus) regions across a variety of positive
and negative emotions such as happiness, anxiety, anger,
sadness, disgust (for reviews, see Borod, 2000; Lane &
Nadel, 2000).
A separate body of psychophysiological research has
sought to identify patterns of autonomic nervous system
*
Corresponding author. Present address: Fachbereich I—Psychologie, Universit€
at Trier, Universit€atsring 15, Trier 54286, Germany.
Fax: +49-651-201-3956.
E-mail address: [email protected] (D. Hagemann).
(ANS) correlates of emotion. Although several investigations have noted emotion-specific autonomic response
patterns (e.g., Ekman, Levenson, & Friesen, 1983; Sinha, Lovallo, & Parsons, 1992), the majority of studies
suggest greater similarities than differences among
physiological activation patterns during various emotional states (for reviews see Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000; Neumann & Waldstein,
2001; Stemmler, 1996).
Study of the linkage between central and autonomic
correlates of emotion is relevant to numerous fields of
investigation including affective neuroscience, neurocardiology, psychophysiology, and behavioral medicine.
Yet, relatively few studies have simultaneously examined
CNS and ANS responses during emotion. In this paper,
we provide an overview of such investigations. Previously, it has been suggested that the right hemisphere
may be dominant in eliciting autonomic responses during
emotion (e.g., Borod & Madigan, 2000; Gainotti, 1989;
Wittling & Roschmann, 1993). However, others have
proposed more complex models of association between
emotion-related central and autonomic response patterns
(Lane & Jennings, 1995; Lane & Schwartz, 1987; Thayer
0278-2626/03/$ - see front matter Ó 2003 Elsevier Science (USA). All rights reserved.
doi:10.1016/S0278-2626(03)00011-3
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D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
& Lane, 2000); many of these models focus on both
cortical and subcortical interconnections (such as frontal–subcortical systems). We present results from the
literature on concomitant CNS and ANS response to
emotional stimuli to suggest the viability of the latter
position. We discuss findings from lesion studies, visual
half field studies, and investigations that have directly
measured CNS activity with the spontaneous electroencephalogram (EEG), evoked potentials (EPs), or neuroimaging techniques, along with measures of ANS
activation. We also highlight a recent model of neurovisceral integration (Thayer & Lane, 2000) to enhance the
findings of the present review. This model relies on
principles of dynamical systems to suggest that different
neural networks are flexibly recruited according to situational demands to integrate the central and autonomic
response to emotional stimuli. We use findings from our
overview of the CNS/ANS literature and the theoretical
position of the model of neurovisceral integration to
provide suggestions for future research directions.
Prior to the review of relevant studies, some remarks
on the definition of ‘‘emotion’’ and additional technical
issues may be helpful. First, defining ‘‘emotion’’ has
been a controversial issue, both historically (e.g., Epstein, 1984), and currently (e.g., Scherer, 2000). For the
purpose of the present review, we use a working definition that focuses on the functional aspects of emotions
(e.g., Frijda, 1986, 1988; Levenson, 1988; see Thayer &
Lane, 2000): Emotions may be characterized as an organismic response to an environmental event that facilitates the rapid mobilization for action. This response
involves multiple systems of the organism, such as cognitive, behavioral, and autonomic sub-systems. When
these response systems are efficiently coordinated, they
allow for goal-directed behavior in the service of flexible
adaptation of the organism to changing environmental
demands.
Second, several researchers have classified emotional
responses in terms of a number of discrete ‘‘basic emotions’’ such as surprise, interest, happiness, rage, fear,
sadness, and disgust (e.g., Ekman, 1984; Izard, 1977;
Tomkins, 1962). In contrast, other investigators have
argued that emotions—at least on the level of subjective
experience—may be more parsimoniously described by
only two dimensions, which are ‘‘valence’’ (pleasant–
unpleasant) and ‘‘arousal’’ (low–high intensity) (e.g.,
Larsen & Diener, 1992; Russell, 1980). Several researchers have suggested that these two dimensions are
hierarchically related to discrete emotions (e.g., Diener,
Smith, & Fujita, 1995; Russell & Barrett, 1999). Nonetheless, these different theoretical orientations have given rise to different emotion induction procedures for
experimental research (for general overviews, see Gerrards-Hesse, Spies, & Hesse, 1994; Oatley & Jenkins,
1996), and concomitant physiology has been contrasted
in various experiments between basic emotions, or be-
tween pleasant and unpleasant states. For example, a
variety of discrete emotions such as happiness, sadness,
anger, fear, and disgust have been elicited with procedures such as presentation of film clips (Lane, Reiman,
Ahern, & Thayer, 2000), presentation of pictures of respective facial expressions (Schneider et al., 1995), recall
and re-experience of personal life episodes (Waldstein
et al., 2000), anticipation of electric shock (Slomine,
Bowers, & Heilman, 1999), or hypnotic induction (de
Pascalis, Ray, Tranquillo, & DÕAmico, 1998). In contrast, pleasant and unpleasant emotions have typically
been induced by the presentation of affective slides (e.g.,
Cuthbert, Schupp, Bradley, Birbaumer, & Lang, 2000;
Lane et al., 1997; Palomba, Angrilli, & Mini, 1997).
Third, the studies described in this review have used a
variety of variables to measure ANS activity. The ANS
has two main branches—the sympathetic and parasympathetic (vagal) nervous systems—that innervate visceral
organs, blood vessels, and glands, and which exert opposite effects on the innervated organs (for an overview,
see Lovallo & Sollers, 2000). The most frequently used
measure of ANS activity is heart rate (HR), which is
antagonistically affected by sympathetic and parasympathetic activity. This dual influence renders considerable ambiguity to the interpretation of HR responses,
but inclusion of other cardiovascular measures can help
to avoid this problem: HR variability and particularly
its high frequency component primarily reflect cardiac
parasympathetic activity whereas measures of myocardial performance indicate primarily b-adrenergic sympathetic activity. Another widely used ANS measure is
blood pressure, which is also influenced by sympathetic
and parasympathetic activity, and skin conductance
response (SCR), which primarily reflects sympathetic
activity.
2. Studies of CNS and ANS correlates of emotion
2.1. Lesion studies
Most lesion studies have contrasted autonomic responses in individuals with right versus left hemispheric
brain lesions. Results suggest a critical role of the right
hemisphere in mediating the ANS response to emotional
stimuli. In this regard, many, though not all (e.g., Slomine et al., 1999), studies demonstrated a diminished
SCR or HR response to pleasant or unpleasant stimuli
in right brain-damaged patients compared with left
brain-damaged patients or control subjects (Andersson
& Finset, 1998; Caltagirone, Zoccolotti, Originale, Daniele, & Mammucari, 1989; Heilman, Schwartz, &
Watson, 1978; Meadows & Kaplan, 1994; Morrow,
Vrtunski, Kim, & Boller, 1981; Zoccolotti, Caltagirone,
Benedetti, & Gainotti, 1986; Zoccolotti, Scabini, &
Violani, 1982).
D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
In contrast, several recent investigations that examined patients with more distinct cerebral lesions suggest
that a right/left distinction in hemispheric dominance for
central and autonomic linkages during emotion is too
simplistic. Tranel and Damasio (1994) found that bilateral lesion of the ventromedial prefrontal region,
unilateral lesion of the right inferior parietal region, and
unilateral left or right lesion of the anterior cingulate
gyrus were associated with a diminished SCR to emotional stimuli. This observation suggests that structures
of both hemispheres are important sites for the neural
networks that link emotional stimuli to ANS responses.
Bechara et al. (1995) found that bilateral lesion of the
amygdala prevented the acquisition of a conditioned
aversive SCR. However, other studies have suggested a
lack of involvement of the amygdala, or hippocampal
regions, in the SCR to emotional stimuli (Tranel &
Damasio, 1989; Tranel & Hyman, 1990).
However, there are problems with lesion studies. For
example, lesion studies are often limited by small sample
sizes. In addition, because naturally occurring lesions
typically do not respect neuroanatomical boundaries (see
Kolb & Taylor, 2000), these types of investigations yield
interpretive difficulties with respect to definitive localization of function. As well, the considerable plasticity of
the brain allows post-lesion relocation of functions,
which also hampers the interpretation of findings.
2.2. Visual half field studies
Central and autonomic responses have also been examined in visual half field studies in normal subjects (for
a review, see Wittling, 1995). In these studies, a visual
stimulus is presented selectively to the right or left
hemisphere and the ANS response is measured. Similar
to the lesion studies, several investigations in this area
also suggested a right-hemispheric dominance for HR
responses to (or in anticipation of) unpleasant stimuli
(Dimond & Farrington, 1977; Hugdahl, Franzon, Andersson, & Walldebo, 1983; Spence, Shapiro, & Zaidel,
1996), although findings related to cardiovascular response to pleasant stimuli were inconsistent (Dimond &
Farrington, 1977; Wittling, 1990).
In contrast, several recent visual half field studies
challenge the hypothesis of right-hemispheric dominance for ANS responses. Some preliminary evidence
has suggested a right hemispheric dominance for emotion-induced sympathetic nervous system response (as
measured by various indices of myocardial function),
and a left hemisphere dominance for the parasympathetic response (as assessed by HR variability) (Wittling,
Block, Genzel, & Schweiger, 1998a; Wittling, Block,
Schweiger, & Genzel, 1998b). Unfortunately, visual half
field studies are limited in number. As well, this research
approach does not allow for a localization of function
within the cerebral hemispheres.
81
2.3. Spontaneous electroencephalography (EEG) studies
A promising approach for the study of central and
autonomic integration in emotion utilizes the spontaneous EEG to localize cortical activation while assessing
an index (or indices) of autonomic function. In a recent
investigation of self-generated happy and sad emotions
and a relaxation condition, de Pascalis et al. (1998)
found that bilateral arousal at the midfrontal cortex,
arousal asymmetry at the precentral cortex (i.e., rightsided asymmetry during sadness and left-sided asymmetry during relaxation), and HR responses all followed
the same response pattern across all conditions. Both
midfrontal and relative right-sided precentral cortical
activation and HR were largest in the sad and smallest
in the relaxation condition. However, there was no cooccurrence of cortical arousal and HR across the three
conditions for parietal sites.
Further studies extended these findings. Schmidt,
Fox, Schulkin, and Gold (1999) found that shy, as
compared to non-shy, children showed a greater increase in right midfrontal cortical activation and a
greater increase in HR during a task designed to induce
self-presentation anxiety. However, no group differences
were noted in the left midfrontal, parietal, and occipital
scalp regions, or in a measure of cardiac vagal tone.
Demaree, Harrison, and Rhodes (2000) found increases
in bilateral frontal cortical activity and HR immediately
before and after a cold pressor test in high hostile, but
not low hostile, men. In a recent study of young adults,
Waldstein et al. (2000) noted positive correlations between left and right midfrontal cortical activation and
HR during an anger recall condition. Subjects who
displayed a lateralized right midfrontal cortical activation response during anger-inducing tasks also showed
enhanced blood pressure responses. In addition, exploratory analyses indicated that men who showed a
lateralized left midfrontal cortical activation response
during happiness-inducing tasks also displayed the
greatest concomitant increase of systolic blood pressure
and HR. Davidson, Marshall, Tomarken, and Henriques (2000) examined social phobics and normal controls during anticipation of public speaking. The social
phobics showed increased state anxiety and increased
relative right-sided hemispheric activity during anticipation of the speech, whereas controls showed no substantive changes. However, the corresponding increase
in HR and blood pressure during anticipation was
similar in both groups, which suggests a lack of correspondence between CNS and ANS measures in this
study. Using a very different experimental paradigm,
Gilbert et al. (1999) noted that one month of smoking
abstinence was associated with decreased cortical activation, particularly at bilateral parietal sites, and a decreased HR. However, there were no significant changes
in positive or negative mood.
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D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
In sum, the spontaneous EEG studies have employed
very different types of samples and have utilized disparate experimental paradigms. It therefore is not surprising that the findings are somewhat heterogeneous.
Nonetheless, preliminary evidence suggests a positive
association between an increased bilateral or right-sided
activation of the anterior cortex and increased HR or
systolic blood pressure in unpleasant emotional states.
Interestingly, none of these studies observed similar associations for posterior sites. However, the evidence for
pleasant emotional states is not consistent, and preliminary evidence suggests the possibility of sex differences. These findings require replication before definitive
interpretations are tenable. In addition, major limitations of the spontaneous EEG include the inability to
record subcortical activity, low spatial resolution, and
mediocre temporal resolution (in the second range).
2.4. Evoked potential studies
Two recent studies evaluated evoked potential (EP)
and autonomic response to emotional stimuli. EP allows
a registration of brain activity with a temporal resolution in the millisecond range. Palomba et al. (1997)
noted a large positive correlation between the amplitude
of the electrocortical response at vertex (averaged across
a time range between 600 and 900 ms after picture onset)
and HR deceleration during presentation of pleasant,
unpleasant, and neutral pictures. In another study,
Cuthbert et al. (2000) noted that the amplitude of the
electrocortical response (averaged across anterior and
posterior sites and across a time range between 400 and
1000 ms after picture onset) to pleasant, unpleasant,
and neutral pictures was associated with an increased
SCR, but not with the HR response. The contradictory
findings of these two studies do not permit conclusions
at present. Although EP methods have superior temporal resolution compared with other measures of CNS
activity, EPs are also not well suited for the registration
of subcortical activity, and have a low spatial resolution.
2.5. Neuroimaging studies
Major advantages of neuroimaging methodology
include the co-registration of cortical and subcortical
activity and good spatial resolution. Several recent investigations simultaneously collected measures of regional cerebral blood flow with 15 O-water positron
emission tomography (PET), and measures of ANS activation during the induction of emotions. Schneider
et al. (1995) found that sad and happy moods, induced by
a combined imagination and picture presentation task,
were associated with different patterns of regional brain
activation, but similar HR accelerations. There were, in
addition, no significant correlations between cerebral
blood flow and HR. Soufer et al. (1998) recorded HR and
blood pressure during a neutral control task and an unpleasant emotional state that was induced with a mental
stress task. Subjects who showed an increased rate pressure product (which is predominantly due to sympathetic
activity) during the emotional state also showed increased brain activation in the cerebellum, the periaqueductual gray, right inferior frontal gyrus, and middle
frontal gyrus/orbitofrontal cortex. Lane et al. (1997)
noted that both pleasant and unpleasant picture presentation were associated with greater activation of left
prefrontal cortex, left thalamus, left hypothalamus, and
left midbrain structures compared with neutral picture
presentation. These valence-independent effects were
accompanied by greater SCR to pleasant and unpleasant
pictures than to neutral stimuli. In a further investigation, Lane, Chua, and Dolan (1999) examined separately
the effects of valence and arousal on regional blood flow
and autonomic activity. Irrespective of valence, highly
arousing stimuli (relative to low arousing stimuli) elicited
both greater SCR, in addition to activation in the medial
prefrontal cortex, right anterior temporal cortex, right
extrastriate cortex, as well as in the left amygdala and left
thalamus. More recently, Damasio et al. (2000) induced
sadness, happiness, anger, and fear with recall of personal life experience, and compared simultaneously registered PET, HR, and SCR with a neutral control
condition. In addition to a multitude of emotion-specific
effects on regional blood flow, there was common activation during all four emotions (compared with the
neutral state) in the right insula, the left midbrain, and the
left mesial cerebellum, in addition to a common deactivation in the right lateral frontal lobe. Increases in HR
and SCR were also noted during sadness, happiness,
anger, and fear as compared to the neutral control condition. Lane et al. (2000) induced happiness, sadness, and
disgust using film clips and personal recall tasks. HR
variability was correlated with regional brain activation
during the emotion conditions, a neutral condition, and
the subtraction of neutral from emotion conditions. Of
particular note, a positive correlation between HR variability and regional brain activation in the medial prefrontal cortex and the left posterior orbitofrontal/
anterior insular cortex was found for the subtraction
comparison. More specifically, emotional arousal was
associated with a decrease in HR variability and concomitant decreases in brain activation in these regions.
To date, relatively few studies have simultaneously
measured CNS activation using neuroimging procedures
and ANS activity during emotional states. Nonetheless,
the preliminary evidence suggests a co-occurrence of left
subcortical activation and increased SCR during both
pleasant and unpleasant emotional states. These subcortical structures comprise the amygdala, thalamus,
and hypothalamus, in addition to midbrain regions of
the left hemisphere. For cortical structures, however,
such lateralization is less clear. Some findings point to a
D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
co-occurrence of greater relative left-sided activation of
the frontal lobe and increased SCR during pleasant and
unpleasant emotion. However, other findings suggest a
co-occurrence of right frontal lobe, insular, anterior
temporal lobe, and extrastriate cortical activation and
increased SCR or rate pressure product during pleasant
and unpleasant states. Considered together, these findings again indicate that a left/right dichotomy is too
simplistic to describe CNS/ANS relations in emotion,
and suggest that localization on the anterior–posterior
and the cortical–subcortical dimensions is also important. Interestingly, the preliminary evidence also suggests that the co-occurrence of CNS and ANS activity
may be mediated by the arousal component of emotional stimuli, rather than by valence. These observations require replication, particularly because many of
these studies are limited by relatively small sample sizes
(particularly in relation to the number of relevant variables), which hampers statistical conclusions. Although
the spatial resolution of neuroimaging methods is good
compared with EEG and EP methods, PET has a low
temporal resolution (in the minute range).
3. Conclusion
The data reviewed above support two primary conclusions. First, there is ample support for the notion that
numerous cortical and subcortical regions show co-occurring activity with ANS responses in emotion. Such a
coupling between CNS and ANS activity may be inferred for frontal, temporal, parietal, and anterior cingulate cortices together with subcortical structures
including the amygdala, thalamus, hypothalamus, and
the midbrain. In this regard, lesion studies indicate that
the ventromedial prefrontal region, the right inferior
parietal region, and the anterior cingulate gyrus are
important sites for the neural networks that link pleasant and unpleasant stimuli to the SCR (Tranel &
Damasio, 1994), and that selective bilateral lesions of
the amygdala prevent the acquisition of conditioned
aversive SCR (Bechara et al., 1995). In addition, spontaneous EEG studies suggest a positive association between an increased bilateral or right-sided activation of
the anterior cortex and increased HR or systolic blood
pressure in unpleasant emotional states (de Pascalis
et al., 1998; Schmidt et al., 1999; Waldstein et al., 2000).
Finally, neuroimaging evidence reveals a co-occurrence
of activation in cortical (frontal, insular, and anterior
temporal), subcortical (amygdala, thalamus, and hypothalamus), and midbrain structures and increased SCR
and HR during pleasant and unpleasant emotional
states (Damasio et al., 2000; Lane et al., 1999; Lane
et al., 2000; Lane et al., 1997). Importantly, although the
observed covariation of CNS and ANS activity across
different emotion induction tasks is suggestive, it must
83
be noted that definitive conclusions are hampered by the
limited number of emotional states assessed, and the
absence of appropriate statistics to quantify and directly
test for correspondence in CNS and ANS responses (for
exceptions, see Cuthbert et al., 2000; Lane et al., 2000;
Palomba et al., 1997; Schneider et al., 1995; Soufer et al.,
1998; Waldstein et al., 2000). In addition, it is important
to note that there is variability in findings across studies.
Second, results of the studies reviewed herein suggest
that a simple left/right dichotomy with respect to hemispheric specialization for the autonomic component of
the emotional response is probably untenable. The empirical data suggest that cortical and subcortical asymmetries in the CNS/ANS processing of emotional
information may be reversed. The lesion and spontaneous EEG studies reviewed above provide some evidence
for right-sided cortical involvement in ANS responses to
unpleasant stimulation (de Pascalis et al., 1998; Schmidt
et al., 1999; Tranel & Damasio, 1994; Waldstein et al.,
2000). In contrast, results of neuroimaging studies suggest a greater involvement of left-hemispheric subcortical
structures (e.g., amygdala, hypothalamus, and thalamus)
in ANS responses to emotional stimuli irrespective of
valence (Damasio et al., 2000; Lane et al., 1999; Lane
et al., 1997). It thus appears that neuroimaging studies
generally point to left subcortical activation during
emotional arousal, whereas electrophysiological evidence
suggests right cortical activation at least for unpleasant
emotion.
Such a reversal of cortical/subcortical activation
asymmetry may be explained by the joint function of
two inhibitory mechanisms. Specifically, the mechanism
of ipsilateral inhibition (e.g., Tucker, 1981; Tucker,
1984) suggests that activation of a cortical region results
in inhibition of efferent subcortical structures. This is
related to Hughlings JacksonÕs classic principle of ‘‘hierarchic integration through inhibition’’ (Jackson, 1879;
Tucker, Derryberry, & Luu, 2000). In addition, the
mechanism of contralateral inhibition (e.g., Sackheim
et al., 1982) suggests that activation of a cortical area
leads to an inhibition of homologous contralateral cortex. The parallel functioning of both mechanisms readily
implies a reversal of cortical and subcortical activation
asymmetries as is suggested in this review (see Liotti &
Tucker, 1995; for a combination of these mechanisms).
However, the present evidence for the proposed reversal
of cortical/subcortical activation asymmetry in emotion
should be explicitly tested in future studies.
We suggest that the present conclusions, derived from
the extant empirical literature, can be enriched by consideration of a recent theoretical model of neurovisceral
integration in emotion. This model was elaborated by
Thayer and Lane (2000), who proposed a network of
neural structures that generate, receive, and integrate
internal and external information in the service of goaldirected behavior and organism adaptability. One such
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D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
functional unit is the central autonomic network (CAN;
Benarroch, 1993, 1997). Functionally, this network is an
integrated component of an internal regulation system
through which the brain controls visceromotor, neuroendocrine, and behavioral responses that are critical for
goal-directed behavior and adaptability (Benarroch,
1993). Structurally, the CAN involves a number of
structures throughout the neuraxis including the anterior cingulate, insular, and ventromedial prefrontal
cortices, the central nucleus of the amygdala, the paraventricular and related nuclei of the hypothalamus,
the periaquaductal gray matter, the parabrachial nucleus, the nucleus of the solitary tract (NTS), the nucleus
ambiguus, the ventrolateral medulla, the ventromedial
medulla, and the medullary tegmental field. These
structures are reciprocally interconnected such that information flows in both directions—top-down and bottom-up. The primary output of the CAN is mediated
through the preganglionic sympathetic and parasympathetic neurons. These neurons innervate the heart via
the stellate ganglia and the vagus nerve. Interestingly,
many of the CAN brain regions have been found to be
associated with autonomic responses in the literature
reviewed above.
The CAN also has many features of a dynamical
system. There is a growing consensus both inside and
outside of cognitive neuroscience that living organisms
are self-organizing dynamical systems (e.g., van Gelder,
1998). This has important implications for attempts to
localize specific functions to specific structures. First,
dynamical systems flexibly recruit system components
into context specific functional units. Thus any given
system element or structure may serve numerous but not
necessarily fixed functions. Second, there is considerable
overlap between the functions and structures associated
with a wide range of behaviors. For example, in the
context of a system designed to maximize adaptability in
the service of goal directed behavior, cognition, emotion, and physiological activities must be coordinated
and built upon the same neural Ôwetware.Õ Discrete behaviors and functions emerge when distributed activity
across system levels is recruited into functional networks
to meet environmental challenges and task demands.
And third, in the context of a dynamical system, inhibitory processes may hold particular importance for
flexible system responding. Unlike the prevailing homeostatic model, dynamical systems models propose
that the system normally functions far from equilibrium.
Accordingly, from a dynamical systems perspective,
emotional (or other) states may reflect modes of relative
stability that occur in the constant flow of organism–
environment interactions.
Because the components of the CAN are reciprocally
interconnected, this allows for continuous positive and
negative feedback interactions and integration of autonomic responses. Next, the CAN comprises a number of
parallel, distributed pathways, which allows for multiple
avenues to a given autonomic response (e.g., increased
sympathetic or decreased parasympathetic activity or
any combination of the two). Moreover, within the
CAN, both direct and indirect pathways can modulate
the output to the preganglionic sympathetic and parasympathetic neurons. Furthermore, the activity of the
CAN is state dependent and thus sensitive to initial
conditions (see Glass & Mackey, 1988).
The model of neurovisceral integration proposes that
the CAN (or related systems that have been identified by
other researchers such as the anterior executive region of
Devinsky, Morrell, & Vogt, 1995; or the ‘‘emotion circuit’’ of Damasio, 1998) constitutes a network of CNS
structures that is associated with the processes of response organization and selection, and serves to modulate psychophysiological resources in both emotion
and attention (Friedman & Thayer, 1998; Thayer &
Friedman, 1997). Thus, according to the model, the core
neural ÔwetwareÕ underpinning cognitive, affective, and
physiological regulation may be one and the same.
Additional structures are flexibly recruited in the service
of specific behavioral adaptations. This sparsely interconnected neural network allows for maximal organism
flexibility in adapting to rapidly changing environmental
demands. When this network is either completely uncoupled or rigidly coupled the organism is less able to
dynamically assemble the appropriate neural support
structures to meet a particular demand and is thus less
adaptive.
The main conclusions and caveats of this review, in
conjunction with the model of neurovisceral integration
in emotion, suggest a number of future directions for
research in this new area of affective neuroscience. First,
given the suggestion of widespread cortical and subcortical involvement, and the possibility of reversed
asymmetries on cortical and subcortical levels, research
on central and autonomic integration in emotion should
utilize neuroimaging as the preferred method for assessing CNS activity. Second, there is ample evidence
that the emotional ANS response includes a complex
pattern of sympathetic and parasympathetic activation
(for a review, see Cacioppo et al., 2000), and preliminary
evidence suggests that different ANS components may
have different CNS concomitants (Wittling et al., 1998a,
1998b). Given that frequently used ANS measures like
HR or blood pressure are antagonistically influenced by
the sympathetic and parasympathetic nervous systems
(Berne & Levy, 2001), future research will greatly benefit
from examination of both sympathetic and parasympathetic activity. Furthermore, evaluation of distinct
sympathetic response patterns (i.e., cardiac versus vascular) would be useful.
Third, there is some evidence that men and women
differ in the experience and expression of emotions (see
Hagemann et al., 1999; and the literature cited there),
D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
and preliminary evidence also suggests that the association between CNS and ANS activity during emotional
states might be moderated by sex (Waldstein et al.,
2000). Thus, future studies might further examine this
individual difference variable. Additional dimensions of
individual differences (e.g., personality) might also influence CNS/ANS integration in emotion.
Fourth, although numerous brain regions display
activation during emotion, this does not necessarily
imply that each of these regions has direct involvement
in autonomic responding. In this regard, associations
between individual differences in CNS and ANS responses during emotional states should be directly
quantified and tested, preferably with multivariate
methods (for an example of a cross-conditions correlation approach, see Cuthbert et al., 2000; and for examples of cross-subjects correlations, see Palomba et al.,
1997; Schneider et al., 1995; Waldstein et al., 2000). It
must be noted, however, that multivariate statistics require larger sample sizes than those employed in most of
the studies reviewed above.
Fifth, a main conclusion of the present paper is that
different basic emotions might share common CNS and
ANS concomitants, which are linked to the arousal dimension of emotion. A rigorous test of this notion will
include not only induction variations with respect to
arousal and valence, but will also test the alternative
hypothesis that different basic emotions share only a few
neural (CNS and ANS) concomitants. The envisioned
study on CNS/ANS integration in emotion will therefore sample activity in multiple cortical and subcortical
regions and from several sympathetic and parasympathetic response systems during the induction of several
basic emotions and control conditions. Interrelations
between CNS and ANS activity will then be examined
with multivariate statistics. This integrated approach
will help to consolidate and extend our knowledge
on the physiological concomitants of the emotional response.
Finally, the model of neurovisceral integration in
emotion may have important implications for the study
of central and autonomic integration in emotion. First,
attempts to localize the cortical concomitants of emotion in any simple way may be untenable. The literature
suggests that a number of neural structures and autonomic changes are associated with emotional states.
Indeed, across investigations, sometimes the same central and autonomic activation patterns are associated
with different emotions and sometimes different central
structures and autonomic changes are associated with
the same emotion. These findings can be reconciled in
the context of dynamical systems models where structures dynamically organize to meet the demands of
specific situations. Healthy systems are characterized by
this emotional complexity and diversity whereas unhealthy systems show perseverative activity and a lack of
85
complexity (Friedman & Thayer, 1998; Thayer &
Friedman, 2002). This perseverative activity reflects the
inability of the system to flexibly assemble the necessary
structures into appropriate functional units in response
to changing environmental demands.
Next, different methods are needed to examine the
dynamics of the physiological activity that support
emotional states. The common procedure of averaging
over large periods of time may obscure important cortical and autonomic dynamics that in themselves may be
the distinguishing features of different emotional and
behavioral states (cf. Vaadia et al., 1995). An additional
corollary is that the typical strategy of averaging data
over individuals also obscures the dynamics and specificity associated with individual differences in the physiological correlates of emotion (Friedman, Santucci,
Curtis, & Pumphrey, 1999).
Last, the neural structures that support emotional
behavior need not differ from those that support other
types of behavior. Indeed, behavior of all types is most
certainly built upon the same physiological wetware.
This presents a challenge for researchers to identify experimental paradigms that will allow us to examine the
system in a more fully integrated fashion.
Acknowledgment
The Deutsche Forschungsgemeinschaft supported
this work through Grant Ha 3044/1-1 to the first author.
References
Andersson, S., & Finset, A. (1998). Heart rate and skin conductance
reactivity to brief psychological stress in brain-injured patients.
Journal of Psychosomatic Research, 44, 645–656.
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., &
Damasio, A. R. (1995). Double association of conditioning and
declarative knowledge relative to the amygdala and hippocampus
in humans. Science, 269, 1115–1118.
Benarroch, E. E. (1993). The central autonomic network: Functional
organization, dysfunction, and perspective. Mayo Clinic Proceedings, 68, 988–1001.
Benarroch, E. E. (1997). The central autonomic network. In P. A. Low
(Ed.), Clinical autonomic disorders (2nd ed., pp. 17–23). Philadelphia: Lippincott–Raven.
Berne, R. M., & Levy, M. N. (2001). Cardiovascular physiology. St.
Louis: Mosby.
€ hman, A. (1993). The structure of emotion. Seattle:
Birbaumer, N., & O
Hogrefe and Huber Publishers.
Borod, J. (Ed.). (2000). The neuropsychology of emotion. New York:
Oxford University Press.
Borod, J. C., & Madigan, N. K. (2000). Neuropsychology of emotion
and emotional disorder: An overview and research directions. In J.
C. Borod (Ed.), The neuropsychology of emotion (pp. 3–28). New
York: Oxford University Press.
Cacioppo, J. T., Berntson, G. G., Larsen, J. T., Poehlmann, K. M., &
Ito, T. A. (2000). The psychophysiology of emotion. In M. Lewis,
86
D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
& J. M. Haviland-Jones (Eds.), Handbook of emotions (2nd ed., pp.
173–191). New York: The Guilford Press.
Caltagirone, C., Zoccolotti, P., Originale, G., Daniele, A., & Mammucari, A. (1989). Autonomic reactivity and facial expression of
emotion in brain-damaged patients. In G. Gainotti, & C. Caltagirone (Eds.), Emotions and the dual brain (pp. 204–221). Berlin:
Springer.
Cuthbert, B. N., Schupp, H. T., Bradley, M. M., Birbaumer, N., &
Lang, P. J. (2000). Brain potentials in affective picture processing:
Covariation with autonomic arousal and affective report. Biological
Psychology, 52, 95–111.
Damasio, A. R. (1998). Emotion in the perspective of an integrated
nervous system. Brain Research Reviews, 26, 83–86.
Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto,
L. L. B., Parvizi, J., & Hichwa, R. D. (2000). Subcortical and
cortical brain activity during the feeling of self-generated emotions.
Nature Neuroscience, 3, 1049–1056.
Davidson, R. J., Marshall, J. R., Tomarken, A. J., & Henriques, J. B.
(2000). While a phobic waits: Regional brain electrical and
autonomic activity in social phobics during anticipation of public
speaking. Biological Psychiatry, 47, 85–95.
Demaree, H. A., Harrison, D. W., & Rhodes, R. D. (2000).
Quantitative electroencephalographic analyses of cardiovascular
regulation in low- and high-hostile men. Psychobiology, 28, 420–
431.
de Pascalis, V., Ray, W. J., Tranquillo, I., & DÕAmico, D. (1998). EEG
activity and heart rate during recall of emotional events in
hypnosis: Relationships with hypnotizability and suggestibility.
International Journal of Psychophysiology, 29, 255–275.
Devinsky, O., Morrell, M. J., & Vogt, B. A. (1995). Contributions of
anterior cingulate cortex to behavior. Brain, 118, 279–306.
Diener, E., Smith, H., & Fujita, F. (1995). The personality structure
of affect. Journal of Personality and Social Psychology, 69, 130–
141.
Dimond, S. J., & Farrington, L. (1977). Emotional response to films
shown to the right or left hemisphere of the brain measured by
heart rate. Acta Psychologica, 41, 255–260.
Ekman, P. (1984). Expression and nature of emotion. In K. Scherer, &
P. Ekman (Eds.), Approaches to emotion (pp. 319–343). Hillsdale:
Erlbaum.
Ekman, P., Levenson, R. W., & Friesen, W. V. (1983). Autonomic
nervous system activity distinguishes among emotions. Science,
221, 1208–1210.
Epstein, S. (1984). Controversial issues in emotion theory. Review of
Personality and Social Psychology, 5, 64–88.
Friedman, B. H., & Thayer, J. F. (1998). Autonomic balance revisited:
Panic anxiety and heart rate variability. Journal of Psychosomatic
Research, 44, 133–151.
Friedman, B. H., Santucci, A. K., Curtis, E. M., & Pumphrey, B. G.
(1999). Idiodynamic profiles of cardiovascular activity. Psychophysiology, 36, S52.
Frijda, N. H. (1986). The emotions. Cambridge: Cambridge University
Press.
Frijda, N. H. (1988). The laws of emotion. American Psychologist, 43,
349–358.
Gainotti, G. (1989). The meaning of emotional disturbance resulting
from unilateral brain injury. In G. Gainotti, & C. Caltagirone
(Eds.), Emotions and the dual brain (pp. 147–167). Berlin: Springer.
Gerrards-Hesse, A., Spies, K., & Hesse, F. W. (1994). Experimental
induction of emotional states and their effectiveness: A review.
British Journal of Psychology, 85, 55–78.
Gilbert, D. G., McClernon, F. J., Rabinovich, N. E., Dibb, W. D.,
Plath, L. C., Hiyane, S., Jensen, R. A., Meliska, C. J., Estes, S. L.,
& Gehlbach, B. A. (1999). WWEEG, physiology, and task-related
mood fail to resolve across 31 days of smoking abstinence:
Relations to depressive traits, nicotine exposure, and dependence.
Experimental and Clinical Psychopharmacology, 7, 427–443.
Glass, L., & Mackey, M. C. (1988). From clocks to chaos. Princeton,
NJ: Princeton University Press.
Hagemann, D., Naumann, E., Maier, S., Becker, G., L€
urken, A., &
Bartussek, D. (1999). The assessment of affective reactivity using
films: Validity, reliability, and sex differences. Personality and
Individual Differences, 26, 627–639.
Heilman, K. M., Schwartz, H., & Watson, R. T. (1978). Hypoarousal
in patients with the neglect syndrome and emotional indifference.
Neurology, 28, 229–232.
Hugdahl, K., Franzon, M., Andersson, B., & Walldebo, G. (1983).
Heart-rate responses (HRR) to lateralized visual stimuli. Pavlovian
Journal of Biological Science, 18, 186–198.
Izard, C. E. (1977). Human emotions. New York: Plenum.
Jackson, J. H. (1879). On affections of speech from diseases of the
brain. Brain, 2, 203–222.
Kolb, B., & Taylor, L. (2000). Facial expression, emotion, and
hemispheric organization. In R. Lane, & L. Nadel (Eds.), Cognitive
neuroscience of emotion (pp. 62–83). New York: Oxford University
Press.
Lane, R. D., Chua, P. M.-L., & Dolan, R. J. (1999). Common effects of
emotional valence, arousal and attention on neural activation
during visual processing of pictures. Neuropsychologia, 37, 989–
997.
Lane, R. D., & Jennings, J. R. (1995). Hemispheric asymmetry,
autonomic asymmetry, and the problem of sudden cardiac death.
In R. J. Davidson, & K. Hugdahl (Eds.), Brain asymmetry (pp.
271–304). Cambridge, MA: The MIT Press.
Lane, R. D., & Nadel, L. (Eds.). (2000). Cognitive neuroscience of
emotion. New York: Oxford University Press.
Lane, R. D., Reiman, E. M., Ahern, G. L., & Thayer, J. F. (2000).
Activity in medial prefrontal cortex correlates with vagal component of heart rate variability during emotion. Psychosomatic
Medicine, 62, 1286.
Lane, R. D., Reiman, E. M., Bradley, M. M., Lang, P. J., Ahern, G.
L., Davidson, R. J., & Schwartz, G. E. (1997). Neuroanatomical
correlates of pleasant and unpleasant emotion. Neuropsychologia,
35, 1437–1444.
Lane, R. D., & Schwartz, G. E. (1987). Induction of lateralized
sympathetic input to the heart by the CNS during emotional
arousal: A possible neurophysiologic trigger of sudden cardiac
death. Psychosomatic Medicine, 49, 274–284.
Larsen, R. J., & Diener, E. (1992). Promises and problems with the
circumplex model of emotion. In M. S. Clark (Ed.), Review of
personality and social psychology: Emotion (Vol. 13, pp. 25–59).
Newbury Park: Sage.
Levenson, R. W. (1988). Emotion and the autonomic nervous system:
A prospectus for research on autonomic specificity. In H. L.
Wagner (Ed.), Social psychophysiology and emotion: Theory and
clinical applications (pp. 17–42). Chichester: Wiley.
Liotti, M., & Tucker, D. M. (1995). Emotion in asymmetric corticolimbic networks. In R. J. Davidson, & K. Hugdahl (Eds.), Brain
asymmetry (pp. 389–423). Cambridge, MA: The MIT Press.
Lovallo, W. R., & Sollers III, J. J. (2000). Autonomic nervous system.
In G. Fink (Ed.), Encyclopedia of stress (Vol. 1, pp. 275–284). San
Diego: Academic Press.
Meadows, M. E., & Kaplan, R. F. (1994). Dissociation of autonomic
and subjective responses to emotional slides in right hemisphere
damage. Neuropsychologia, 32, 847–856.
Morrow, L., Vrtunski, P. B., Kim, Y., & Boller, F. (1981). Arousal
response to emotional stimuli and laterality of lesion. Neuropsychologia, 19, 65–71.
Neumann, S. A., & Waldstein, S. R. (2001). Similar patterns of
cardiovascular response during emotional activation as a function
of affective valence and arousal and gender. Journal of Psychosomatic Research, 50, 245–253.
Oatley, K., & Jenkins, J. M. (1996). Understanding emotion. Cambridge, MA: Blackwell.
D. Hagemann et al. / Brain and Cognition 52 (2003) 79–87
Palomba, D., Angrilli, A., & Mini, A. (1997). Visual evoked potentials,
heart rate responses and memory to emotional pictorial stimuli.
International Journal of Psychophysiology, 27, 55–67.
Russell, J. A. (1980). A circumplex model of affect. Journal of
Personality and Social Psychology, 39, 1161–1178.
Russell, J. A., & Barrett, L. F. (1999). Core affect, prototypical
emotional episodes, and other things called emotion: Dissecting the
elephant. Journal of Personality and Social Psychology, 76, 805–
819.
Sackheim, H. A., Greenberg, M. S., Weiman, A. L., Gur, R.,
Hungerbuhler, J. P., & Geschwind, N. (1982). Hemispheric
asymmetry in the expression of positive and negative emotions.
Archives of Neurology, 39, 210–218.
Scherer, K. R. (2000). Psychological models of emotion. In J. C. Borod
(Ed.), The neuropsychology of emotion (pp. 137–162). New York:
Oxford University Press.
Schmidt, L. A., Fox, N. A., Schulkin, J., & Gold, P. W. (1999).
Behavioral and psychophysiological correlates of self-presentation
in temperamentally shy children. Developmental Psychobiology, 35,
119–135.
Schneider, F., Gur, R. E., Mozley, L. H., Smith, R. J., Mozley, P. D.,
Censits, D. M., Alavi, A., & Gur, R. C. (1995). Mood effects on
limbic blood flow correlate with emotional self-rating: A PET study
of oxygen-15 labeled water. Psychiatry Research: Neuroimaging,
61, 265–283.
Sinha, R., Lovallo, W. R., & Parsons, O. A. (1992). Cardiovascular
differentiation of emotions. Psychosomatic Medicine, 54, 422–435.
Slomine, B., Bowers, D., & Heilman, K. M. (1999). Dissociation
between autonomic responding and verbal report in right and left
hemisphere brain damage during anticipatory anxiety. Neuropsychiatry Neuropsychology and Behavioral Neurology, 12, 143–148.
Soufer, R., Bremner, J. D., Arrighi, J. A., Cohen, I., Zaret, B. L., Burg,
M. M., & Goldman-Rakic, P. (1998). Cerebral cortical hyperactivation in response to mental stress in patients with coronary
artery disease. Proceedings of the National Academy of Sciences, 95,
6454–6459.
Spence, S., Shapiro, D., & Zaidel, E. (1996). The role of the right
hemisphere in the physiological and cognitive components of
emotional processing. Psychophysiology, 33, 112–122.
Stemmler, G. (1996). Psychophysiologie der Emotionen. Zeitschrift f€ur
psychosomatische Medizin, 42, 235–260.
Thayer, J. F., & Friedman, B. H. (1997). The heart of anxiety: A
dynamical systems approach. In A. Vingerhoets (Ed.), The (non)
expression of emotions in health and disease (pp. 39–49). Amsterdam: Springer.
Thayer, J. F., & Friedman, B. H. (2002). Stop that! Inhibition,
sensitization and their neurovisceral concomitants. Scandinavian
Journal of Psychology, 43, 123–130.
Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral
integration in emotion regulation and dysregulation. Journal of
Affective Disorders, 61, 201–216.
87
Tomkins, S. S. (1962). Affect, imagery, consciousness. New York:
Springer.
Tranel, D., & Damasio, H. (1989). Intact electrodermal skin conductance response after bilateral amygdala damage. Neuropsychologia,
27, 381–390.
Tranel, D., & Damasio, H. (1994). Neuroanatomical correlates of
electrodermal skin conductance response. Psychophysiology, 31,
427–438.
Tranel, D., & Hyman, B. T. (1990). Neuropsychological correlates of
bilateral amygdala damage. Archives of Neurology, 47, 349–355.
Tucker, D. M. (1981). Lateral brain function, emotion, and conceptualization. Psychological Bulletin, 89, 19–46.
Tucker, D. M. (1984). Lateral brain function in normal and disordered
emotion: Interpreting electroencephalographic evidence. Biological
Psychology, 19, 219–235.
Tucker, D. M., Derryberry, D., & Luu, P. (2000). Anatomy and
physiology of human emotion: Vertical integration of brain stem,
limbic, and cortical systems. In J. C. Borod (Ed.), The neuropsychology of emotion (pp. 56–79). New York: Oxford University
Press.
Vaadia, E., Haalman, I., Abeles, M., Bergman, H., Prut, Y., Slovin,
H., & Aertsen, A. (1995). Dynamics of neuronal interactions in
monkey cortex in relation to behavioural events. Nature, 373, 515–
518.
van Gelder, T. (1998). The dynamical hypothesis in cognitive science.
Behavioral and Brain Sciences, 21, 615–628.
Waldstein, S. R., Kop, W. J., Schmidt, L. A., Haufler, A. J., Krantz,
D. S., & Fox, N. A. (2000). Frontal electrocortical and cardiovascular reactivity during happiness and anger. Biological Psychology,
55, 3–23.
Wittling, W. (1990). Psychophysiological correlates of human brain
asymmetries. Neuropsychologia, 28, 457–470.
Wittling, W. (1995). Brain asymmetry in the control of autonomic–
physiologic activity. In R. J. Davidson, & K. Hugdahl (Eds.), Brain
asymmetry (pp. 305–357). Cambridge, MA: The MIT Press.
Wittling, W., Block, A., Genzel, S., & Schweiger, E. (1998a).
Hemisphere asymmetry in parasympathetic control of the heart.
Neuropsychologia, 36, 461–468.
Wittling, W., Block, A., Schweiger, E., & Genzel, S. (1998b).
Hemisphere asymmetry in sympathetic control of the human
myocardium. Brain and Cognition, 38, 17–35.
Wittling, W., & Roschmann, R. (1993). Emotion-related hemisphere
asymmetry: Subjective emotional responses to laterally presented
films. Cortex, 29, 431–448.
Zoccolotti, P., Caltagirone, C., Benedetti, N., & Gainotti, G. (1986).
Pertubation des responses vegetatives aux stimuli emotionnels au
cours des lesions hemispheriques unilaterales. Encephale, 12, 263–
268.
Zoccolotti, P., Scabini, D., & Violani, C. (1982). Electrodermal
responses in patients with unilateral brain damage. Journal of
Clinical Neuropsychology, 4, 143–150.