Anger: A review of human electrophysiology 1
Anger: A review of human electrophysiology and functional neuroimaging research
Eddie Harmon-Jones
University of Wisconsin – Madison
Address correspondence to:
Eddie Harmon-Jones University of Wisconsin--Madison Department of Psychology 1202 West Johnson Street Madison, Wisconsin 53706-1611 phone: (608) 265-5504 fax: (608) 262-4029 email: [email protected]
Anger: A review of human electrophysiology 2
Evidence from a variety of research approaches has pointed to the importance of
asymmetrical frontal cortical activity in emotional/motivational processes. Much of this
evidence has been obtained with electroencephalographic (EEG) measures of brain
activity, or more specifically, alpha frequency band activity derived from the EEG.
Research has revealed that alpha power is inversely related to regional brain activity
using hemodynamic measures (Cook, O’Hara, Uijtdehaage, Mandelkern, & Leuchter,
1998) and behavioral tasks (Davidson, Chapman, Chapman, & Henriques, 1990).
Additional data from individuals with brain damage supports the research with EEG (e.g.,
Robinson & Downhill, 1995).
In the EEG research, depression has been found to relate to resting frontal
asymmetrical activity, with depressed individuals showing relatively less left than right
frontal brain activity (Jacobs & Snyder, 1996; Schaffer, Davidson, & Saron, 1983).
Moreover, relatively less left frontal activity has been found in individuals who were
previously clinically depressed but were in remission status (Henriques & Davidson,
1990).
Other research has revealed that trait positive affect is associated with greater left
than right frontal brain activity, whereas trait negative affect is associated with greater
right than left frontal brain activity (e.g., Tomarken, Davidson, Wheeler, & Doss, 1992).
Still other research has found that trait behavioral activation sensitivity (BAS) relates to
greater left than right frontal brain activity (Harmon-Jones & Allen, 1997; Sutton &
Davidson, 1997).
Anger: A review of human electrophysiology 3
In addition to the research that suggests that resting baseline frontal asymmetrical
activity relates to other measures of trait emotion and motivation, research has found that
resting baseline frontal asymmetrical activity predicts emotional responses. For example,
individuals with relatively greater right than left frontal activity during baseline recording
sessions report larger negative affective responses to negative emotion-inducing films
(fear and disgust) and smaller positive affective responses to positive emotion-inducing
films (happiness) (Tomarken, Davidson, & Henriques, 1990; Wheeler, Davidson, &
Tomarken, 1993). Moreover, relative right frontal activity at baseline predicts crying in
response to maternal separation in 10-month-old infants (Davidson & Fox, 1989).
Research has also demonstrated that asymmetrical frontal brain activity is
associated with state emotional responses. For instance, Davidson and Fox (1982) found
that 10-month-old infants exhibited increased left frontal activation in response to a film
clip of an actress generating a happy facial expression as compared to a sad facial
expression. Frontal brain activity has been found to relate to facial expressions of positive
and negative emotions, as well. For example, Ekman and Davidson (1993) found
increased left frontal activation during voluntary facial expressions of smiles of
enjoyment. More recently, Coan, Allen, and Harmon-Jones (2001) found that voluntary
facial expressions of fear produced relatively less left frontal activity.
Finally, biofeedback training has been used to manipulate asymmetrical frontal
cortical activity and the effects of this manipulation on emotional responses have been
observed (Allen, Harmon-Jones, & Cavender, 2001). These results suggest that the
frontal asymmetry can be altered using biofeedback training and that this alteration can
affect emotional responses, with an increase in left frontal cortical activity causing more
Anger: A review of human electrophysiology 4
happy emotional facial expressions and an increase in relative right frontal cortical
activity causing more sad emotional facial expressions. Taken together, this research
suggests that asymmetrical frontal cortical activity is causally involved in emotional
responses (for a more detailed review, see Coan & Allen, 2003).
Explanations of the Relationship between Asymmetrical Frontal Activity and
Emotion/Motivation
All of this past evidence can be summarized within one of three theoretical
models. According to the valence model, the left frontal brain region is involved in the
experience and expression of positive emotion and the right frontal brain region is
involved in the expression and experience of negative emotion (e.g., Ahern & Schwartz,
1985; Gotlib, Ranganath, & Rosenfeld, 1998; Heller, 1990; Heller & Nitschke, 1998;
Silberman & Weingartner, 1986). Indeed, research is consistent with this model and it is
widely accepted (e.g., Oatley & Jenkins, 1996; Zajonc & McIntosh, 1992).
According to the motivational direction model, the left frontal brain region is
involved in expression of approach-related emotions and the right frontal brain region is
involved in expression withdrawal-related emotions (Fox, 1991; Harmon-Jones & Allen,
1997; Sutton & Davidson, 1997). Again, the obtained results can be accommodated by
this model. That is, the affects and emotions that have been examined in the research are
all associated with approach or withdrawal motivation. The approach-related emotions
have been found to be associated with relatively greater left frontal activity, whereas the
withdrawal-related emotions have been found to be associated with relatively greater
right frontal activity.
Anger: A review of human electrophysiology 5
According to the valenced motivation model, the left frontal brain region is
involved in the expression and experience of positive, approach-related emotions and the
right frontal brain region is involved in the expression and experience of negative,
withdrawal-related emotions (Davidson, 1998; Tomarken & Keener, 1998). The obtained
results can also be accommodated by this model. That is, the positive affects that have
been examined in the research are all associated with approach motivation, and the
negative affects that have been examined are all associated with withdrawal motivation.
Because the previously conducted research confounded the valence of the
emotion with the direction of motivation, it had been unable to address whether the
frontal asymmetry reflects the valence of the emotion, the direction of the motivation, or
a combination of valence and motivation. Often, positive emotion is associated with
approach-related motivation, whereas negative emotion is associated with withdrawal-
related motivation. Indeed, most contemporary theories of emotion posit that positive
emotion is always associated with approach motivation and that negative emotion is
always associated with negative emotion (Gray, 1994a, 1994b; Watson, 2000; for a
different point of view, see Carver, 2001). However, not all emotions behave in accord
with this assumed relationship between the valence of emotion and direction of
motivation. Anger is one of the best examples of a violation of the relationship, because
anger is negative in valence (e.g., Lazarus, 1991; Watson, 2000), but it often evokes
approach motivation (e.g., Berkowitz, 1999; Darwin, 1872/1965; Plutchik, 1980; Young,
1943).
In addressing the exact emotional/motivation functions of asymmetrical frontal
brain activity, my colleagues and I have examined the emotion of anger, as it is a
Anger: A review of human electrophysiology 6
negative emotion that often evokes approach motivational tendencies. In support of the
motivational direction model over the other two models, recent evidence has suggested
that anger and aggression may be associated with greater left than right frontal cortical
activity. In this chapter, I will review the evidence supportive of such a relationship.
Then, I will briefly consider evidence, seemingly inconsistent with the aforementioned
research, that suggests that aggression is associated with decreased frontal cortical
activity. In the end, I will offer some resolutions to these apparent discrepancies and
suggest some further empirical tests of the relationship between anger, aggression, and
frontal cortical activity.
Anger and Approach Motivation
Before reviewing the research on anger and asymmetrical frontal activity, it is
important to consider whether anger is associated with approach motivation. Several lines
of research suggest that anger elicits behavioral approach or approach motivation
tendencies.
Behavioral Evidence
In the animal behavior literature, a distinction has been made between offensive
or irritable aggression and defensive aggression (Flynn, Vanegas, Foote, & Edwards,
1970; Moyer, 1976). It has been posited that irritable aggression results from anger and
that pure irritable aggression “involves attack without attempts to escape from the object
being attacked” (Moyer, 1976, p. 187). A number of aggression researchers have
suggested that offensive aggression is associated with anger, attack, and no attempts to
escape, whereas defensive aggression is associated with fear, attempts to escape, and
attack only if escape is impossible (Blanchard & Blanchard, 1984; Lagerspetz, 1969;
Anger: A review of human electrophysiology 7
Moyer, 1976). In demonstrating that organisms evidence offensive aggression and that
this is an approach behavior, Lagerspetz (1969) found that under certain conditions mice
would cross an electrified grid to attack another mouse.
With adult humans, Baron (1977) demonstrated that signs of their tormentor’s
pain reinforce angry persons positively. The participants who had been deliberately
provoked by another individual then had a sanctioned opportunity to assault him.
Indications that their first attacks were hurting their target led to intensified aggression
even though the unprovoked participants reduced the intensity of their punishment at
learning of the other’s pain. The initial signs of their victim’s suffering showed the angry
persons they were approaching their aggressive goal and evoked even stronger assaults
from them (see also, Berkowitz, Cochran, & Embree, 1981).
Subsequent to frustrating events, anger may maintain and increase task
engagement and approach motivation. Lewis, Sullivan, Ramsay, and Alessandri (1992)
found that infants who expressed anger during extinction maintained interest during
subsequent relearning, whereas infants who expressed sadness during extinction
evidenced decreased interest during relearning.
Subjective Evidence
Additional support for the idea that anger is associated with approach motivation
comes from research testing the conceptual model that integrated reactance theory with
learned helplessness theory (Wortman & Brehm, 1975). According to this model, how
individuals respond to uncontrollable outcomes depends on their expectation of being
able to control the outcome and the importance of the outcome. When an individual
expects to be able to control outcomes that are important, and those outcomes are found
Anger: A review of human electrophysiology 8
to be uncontrollable, psychological reactance should be aroused. Thus, for individuals
who initially expect control, the first few bouts of uncontrollable outcomes should arouse
reactance, a motivational state aimed at restoring control. After several exposures to
uncontrollable outcomes, these individuals should become convinced that they cannot
control the outcomes and should show decreased motivation (i.e., learned helplessness).
In other words, reactance will precede helplessness for individuals who initially expect
control. In one study testing this model, individuals who exhibited angry feelings (a
manifestation of reactance) in response to one unsolvable problem had better
performance and more approach motivation on a subsequent cognitive task than did
participants who exhibited less anger (Mikulincer, 1988).
Other research has revealed that state anger relates to high levels of self-
assurance, physical strength, and bravery (Izard, 1991), inclinations associated with
approach motivation. Additionally, Lerner and Keltner (2001) found that anger (both trait
and state) is associated with optimistic expectations, whereas fear is associated with
pessimistic expectations. Moreover, happiness was associated with optimism, making
anger and happiness appear more similar to each other in their relationship with optimism
than fear and anger. Although Lerner and Keltner (2001) interpreted their findings as
being due to the appraisals associated with anger, it seems equally plausible that it was
the approach motivational character of anger that caused the relationship of anger and
optimism. That is, anger creates optimism because anger engages the approach
motivational system and produces greater optimistic expectations.
Hormonal and Physiological Evidence
Anger: A review of human electrophysiology 9
Further evidence supporting the conceptualization of anger as involving approach
and not withdrawal comes from research on testosterone, which has been found to be
associated with anger and aggression in humans (e.g., Olweus, 1986). In this research,
testosterone treatments have been found to decrease withdrawal (fear) responses in a
number of species (e.g., Boissy & Bouissou, 1994; Vandenheede & Bouissou, 1993).
Other research has demonstrated that damage to the amygdala, a brain region involved in
defensive behavior, has no effect on offensive aggression but reduces reactivity to
nonpainful threat stimuli (Blanchard & Takahashi, 1988; Busch & Barfield, 1974).
Individual Differences Evidence
Other evidence supporting the idea that anger is associated with an approach-
orientation comes from research on bipolar disorder. The emotions of euphoria and anger
often occur during manic phases of bipolar disorder (Cassidy, Forest, Murry, & Carroll,
1998; Depue & Iacono, 1989; Tyrer & Shopsin, 1982). Both euphoria and anger may be
approach-oriented processes, and a dysregulated or hyperactive approach system may
underlie mania (Depue & Iacono, 1989; Fowles, 1993). Research suggests that
hypomania/mania involves increased left frontal brain activity and approach motivational
tendencies. In this research, it has been found that individuals who have suffered damage
to the right frontal cortex are more likely to evidence mania (see review by Robinson &
Downhill, 1995). Thus, this research is consistent with the view that mania may be
associated with increased left frontal activity and increased approach tendencies, because
the approach motivation functions of the left frontal cortex are released and not restrained
by the withdrawal system in the right frontal cortex. Furthermore, lithium carbonate, a
treatment for bipolar disorder, reduces aggression (Malone, Delaney, Luebbert, Cater, &
Anger: A review of human electrophysiology 10
Campbell, 2000), suggesting that anger and aggression correlate with the other symptoms
of bipolar disorder. In addition, trait anger has been found to relate to high levels of
assertiveness and competitiveness (Buss & Perry, 1992). Finally, trait anger, as measured
by the Buss and Perry (1992) anger subscale, has been found to relate to trait BAS, as
measured by Carver and White’s (1994) questionnaire (Harmon-Jones, in press-a).
While individuals with relatively low left frontal activation are at risk for deficits
in approach motivation and depression, those with relatively high left frontal activation
may evidence excessive approach motivation, leading to increased anger and aggression.
Asymmetrical Frontal Activity and Trait Anger
In all past research on the frontal asymmetry, the valence of the affective style
(positive vs. negative) was confounded with the direction of the motivation (approach vs.
withdrawal). Consequently, scientists have concluded that that the frontal asymmetry
reflects differences in emotional valence (e.g., Ahern & Schwartz, 1985; Gotlib,
Ranganath, & Rosenfeld, 1998; Heller, 1990; Heller & Nitschke, 1998). To address this
confound, Harmon-Jones and Allen (1998) assessed the relationship between resting
frontal asymmetrical activity and anger, an emotion that is negatively valenced but
approach-related. Results indicated that trait anger related to increased left frontal activity
and decreased right frontal activity.
More recently, Harmon-Jones (in press-b) addressed an alternative explanation for
the results of Harmon-Jones and Allen (1998). The alternative explanation suggested that
persons with high levels of trait anger might experience anger as a positive emotion, and
this positive feeling or attitude toward anger could be responsible for anger being
associated with relative left frontal activity. Anger might have been regarded positively
Anger: A review of human electrophysiology 11
because of the subjective feel or evaluation of the emotion. After conducting three studies
that developed a valid and reliable assessment of attitude toward anger, a study was
conducted to assess whether resting baseline asymmetrical activity related to trait anger
and attitude toward anger. Results indicated that anger related to relative left frontal
activity and not attitude toward anger. Moreover, further analyses revealed that the
relationship between trait anger and left frontal activity was not due to anger being
associated with a positive attitude toward anger.
Asymmetrical Frontal Activity and State Anger
Although the Harmon-Jones and Allen (1998) and the Harmon-Jones (in press-b)
studies suggest that anger is related to relative left frontal activity, both studies are
correlational and subject to the interpretational limitations associated with correlational
studies (e.g., a third variable causes the observed relationship). To address these
limitations, experiments have been conducted in which anger is manipulated and its
effects on regional brain activity are examined.
State Anger Induced via Interpersonal Insult and Asymmetrical Frontal Activity
Harmon-Jones and Sigelman (2001) conducted an experiment to assess whether
situationally induced anger would increase relative left frontal activity. Participants were
randomly assigned to a condition in which another person insulted them or to a condition
in which another person treated them in a neutral manner. Immediately following the
treatment, EEG was collected. As predicted, individuals who were insulted evidenced
greater relative left frontal activity than individuals who were not insulted. Additional
analyses revealed that within the insult condition, reported anger and aggression were
positively correlated with relative left frontal activity. Neither of these correlations was
Anger: A review of human electrophysiology 12
significant in the no-insult condition. These results suggest that relative left-frontal
activation was associated with more anger and aggression in the condition in which anger
was evoked. This research thus provides the first demonstration of a relationship between
state anger and relative left frontal activation, a result predicted by models that posit that
the frontal asymmetry reflects motivational direction but not predicted by models that
posit that the frontal asymmetry reflects emotional valence.
The Effect of Coping Potential on Anger-Related Left Frontal Cortical Activity
In the experiments reviewed thus far, it was assumed that anger related to left
frontal cortical activity because anger was associated with approach motivation. In
Harmon-Jones and Sigelman (2001), the experiment was designed in a manner to evoke
anger that was approach oriented. Although most instances of anger involve approach
inclinations, not all forms of anger are associated with approach motivation. To
manipulate approach motivation independently of anger, Harmon-Jones, Sigelman,
Bohlig, and Harmon-Jones (2003) performed an experiment in which the ability to cope
with the anger-producing event was manipulated. Based on past research that has
revealed that coping potential affects motivational intensity (Brehm & Self, 1996), it was
predicted that the expectation of being able to take action to resolve the anger-producing
event would increase approach motivational intensity relative to expecting to be unable to
take action.
In the experiment, university students opposed to a tuition increase were exposed
to an editorial that argued for a tuition increase. They were exposed to this
counterattitudinal message, as a large body of research has suggested that exposure to
such messages evokes negative affect (for a review, see Harmon-Jones, 2000).
Anger: A review of human electrophysiology 13
Conditions differed with regard as to whether it was possible for participants to act to
change the likelihood that tuition will be increased, to manipulate coping potential or the
expectation of acting to change the situation. In the action-possible condition, participants
were told that the increase may occur in the future and that petitions were being
circulated to attempt to prevent the increase. In the action-impossible condition,
participants were told that the tuition increase would definitely occur.
Both conditions evoked significant increases in anger (over baseline) and they
were not significantly different from each other. More importantly and consistent with
predictions, results indicated that participants who expected to engage in the approach-
related action of signing a petition to ameliorate the tuition-increase situation (action-
possible condition) evidenced greater left frontal activity than participants who expected
to be unable to engage in approach-related action. Moreover, within the action-possible
condition, participants who evidenced greater left frontal activity in response to the
tuition increase message also evidenced greater self-reported anger, providing support for
the idea that anger is often an approach-related emotional response. In the condition
where action was not possible, greater left frontal activity did not relate to greater anger.
This is because, although anger usually leads to approach motivation, when action is not
possible, approach motivation should remain low, even if angry feelings are high. Finally,
within the action-possible condition, participants who evidenced greater left frontal
activity in response to the tuition increase message were more likely to engage in
behaviors that would reduce the possibility of the tuition increase (i.e., they were more
likely to sign the petition and to take petitions with them for others to sign). This finding
Anger: A review of human electrophysiology 14
suggests that greater approach motivation, as reflected in greater left frontal cortical
activity, was associated with more action to correct the negative situation.
The research of Harmon-Jones, Sigelman et al. (2003) supports the hypothesis
that the left frontal cortical region is involved in approach motivation rather than positive
affect. Moreover, the results suggest that the left frontal region is most accurately
described as a region sensitive to motivational intensity. That is, it was only when anger
was associated with an opportunity to behave in a manner to resolve the anger-producing
event that participants evidenced the increased relative left frontal activation.
Proneness toward Hypomania/Mania and Anger-Related Left Frontal Cortical Activity
The reviewed research suggests that anger is related to relative left frontal cortical
activity because anger is associated with approach motivation. Consequently, individuals
with greater trait approach motivation may be particularly likely to evidence greater left
frontal activity in response to an anger-provoking situation, as they feel motivated to
redress the anger-provoking situation. In contrast, individuals with lower trait approach
motivation may be particularly unlikely to evidence greater left frontal activity and may
instead respond with lower left frontal activity, as they feel hopeless to redress the anger-
provoking situation. To examine these ideas, Harmon-Jones, Abramson, Sigelman,
Bohlig, Hogan, and Harmon-Jones (2002) exposed individuals with high and low trait
approach motivation to an anger-producing situation. Based on the observed link between
hypomania/mania and increased approach motivation (Depue & Iacono, 1989; Meyer et
al., 1999), we predicted that proneness toward mania would be related to increased
relative left frontal activity in response to an anger-evoking event. In contrast, based on
the link between depression and decreased approach motivation (Depue & Iacono, 1989;
Anger: A review of human electrophysiology 15
Fowles, 1993; Henriques & Davidson, 1990), we predicted that proneness toward
unipolar depression would be related to decreased relative left frontal activity in response
to the anger-invoking event. To assess these individual differences characteristics among
a sample of unselected undergraduate students, we used the General Behavior Inventory,
which was developed to identify individuals who are at risk for developing these
disorders (Depue & Klein, 1988; Depue, Krauss, Spoont, & Arbisi, 1989). Results
indicated that tendencies toward hypomania/mania related to increased left frontal
activity, and that tendencies toward unipolar depression related to decreased left frontal
activity following exposure to the anger-provoking radio editorial. In these analyses,
resting, baseline relative left frontal activity was statistically controlled, suggesting that
the effects were specific to when anger was aroused.
Sympathy Reduces Anger-Related Left Frontal Activity
Whereas the reviewed evidence links approach anger to relative left frontal
activity, it is important to establish that manipulations that reduce angry approach
behaviors also reduce relative left frontal activity. To address this issue, we tested
whether sympathy would reduce the relative left frontal activity typically observed during
anger. Past research has suggested that experiencing sympathy for another individual can
reduce aggression toward that individual (e.g., see review by Miller & Eisenberg, 1988).
We hypothesized that sympathy may reduce aggression by reducing the relative left
frontal activity associated with anger. To test this hypothesis, college students were told
that the study concerned personality, perception, and brain activity, and that they and
another student would be writing essays and evaluating each other based on the essays.
Participants then wrote a persuasive essay arguing either for or against a 10% tuition
Anger: A review of human electrophysiology 16
increase. Then, the experimenter returned to the participants’ room and handed them a
folder containing a reading perspective, an essay, and a questionnaire.
The reading perspective instructions asked participants to remain completely
objective (low sympathy) or to try to imagine how the other person must feel (high
sympathy), as in much past sympathy research (Batson, 1991, 1998; Harmon-Jones,
Peterson, & Vaughn, 2003; Stotland, 1969). The participant then read the essay
ostensibly written by the other participant. In the essay, the other participant described
his/her difficulties with having Multiple Sclerosis.
Following the reading of the essay, the participant received an evaluation of
his/her essay ostensibly written by other participant. The evaluation contained either
neutral ratings and comments (no insult) or insulting ratings and comments (insult).
Immediately after feedback manipulation, EEG was collected. Then, the participant
completed questionnaires assessing impressions of the other participant and emotions.
Results indicated that the insult evoked greater left frontal activity but only when
high levels of sympathy were not first evoked for the insulting person. Additional
comparisons revealed that the high sympathy/insult condition produced greater relative
left frontal activity than every other condition. Thus, when participants first experienced
sympathy for the target person, they did not evidence increased left frontal activity when
insulted. The experiment thus suggested that the alteration of relative left frontal activity
via sympathy can reduce angry aggression.
Manipulation of Left Frontal Cortical Activity and Attentional Processing of Anger
In addition to the reviewed evidence, other research is consistent with the
hypothesis that anger is associated with left frontal activity. For example, d’Alfonso, van
Anger: A review of human electrophysiology 17
Honk, Hermans, Postma, and de Haan (2000) recently used slow repetitive transcranial
magnetic stimulation (rTMS) to inhibit the left or right prefrontal cortex. They found that
rTMS applied to the right prefrontal cortex caused selective attention towards angry faces
whereas rTMS applied to the left prefrontal cortex caused selective attention away from
angry faces. Because slow rTMS produces inhibition of cortical excitability, these results
suggests that the rTMS applied to the right prefrontal cortex decreased its activation and
caused the left prefrontal cortex to become more active. The same holds true for the
rTMS applied to the right prefrontal cortex and activation of the left prefrontal cortex.
The increase in left prefrontal activity led participants to attentionally approach angry
faces, as in an aggressive confrontation. In contrast, the increase in right prefrontal
activity led participants to attentionally avoid angry faces, as in a frightening
confrontation. The interpretation of these results, which d’Alfonso et al. advanced,
concurs with other research that has demonstrated that attention toward angry faces is
associated with high levels of self-reported anger and that attention away from angry
faces is associated with high levels of cortisol (van Honk, Tuiten, de Haan, van den Hout,
& Stam, 2001; Van Honk, Tuiten, Van den Hout, Koppeschaar, Thijssen, & de Haan,
1998; van Honk, Tuiten, Verbaten, van den Hout, Koppeschaar, Thijssen, & de Haan,
1999), which is associated with fear.
Research on Anger Using Other Brain Imaging Methods
Whereas the above-reviewed research has revealed that the left frontal cortical
region is involved in approach motivation and anger, it is limited in that EEG is the sole
imaging method used. While EEG possesses excellent temporal resolution, its spatial
resolution is limited. A search of the literature revealed two experiments that had
Anger: A review of human electrophysiology 18
examined the effects of anger on brain activity measured with brain imaging methods
other than EEG.1 Both experiments utilized positron emission tomography (PET). One
used oxygen-15-labeled carbon dioxide to study normalized regional cerebral blood flow
during anger as compared to a neutral control state (Dougherty et al., 1999). In the
experiment, eight healthy men provided a written description of a time when they were
the most angry they had been in their life. The neutral scripts were generated by the
experimenters (i.e., going for a walk, cooking dinner). Based on the anger material
provided by the participant and the experimenter-generated neutral information, the
experimenter created a script in the second person and then audiotaped it in a neutral
voice for playback in the lab. The scripts were 30-40 sec long. Other emotions were
activated in a similar manner but the results were not published in the report. Emotion
induction time was counterbalanced across participants. Before each scan, the participant
was told to close his eyes, listen to the script, and “imagine the event portrayed as vividly
as possible, as if he was actually participating in the event, rather than just ‘watching
himself’ in it.” (p. 467). Participants were asked to recall and imagine the event for 60 sec
following the script audiotape. Positron emission tomography (PET) data were collected
during this time period. The anger and neutral conditions did not differ on heart rate, skin
conductance, or frontalis muscle activity, even though past research would suggest that
differences between conditions should emerge (e.g., Jaencke, 1996; Lavoie, Miller,
Conway, & Fleet, 2001). Perhaps anger was not evoked or perhaps the anger was not
sufficiently strong to affect these variables. However, the anger condition reported
greater anger than the neutral condition. The PET results revealed that as compared to
neutral imagery, anger imagery caused an increase in the left orbital frontal cortex, the
Anger: A review of human electrophysiology 19
right anterior cingulate cortex, the bilateral anterior temporal poles, left precentral gyrus,
bilateral medial frontal cortex, and bilateral cerebellum. No significant differences
emerged between conditions in the amydala or insular cortex.
Thus, the increase in activity in the left orbital frontal cortex is consistent with the
anger research results obtained using EEG. However, Dougherty et al. (1999) interpreted
the increase in left orbital frontal cortical activity as corresponding “to inhibition of
aggressive behavior in the face of anger.” (p. 471). While this interpretation is consistent
with some speculations of the role of the left orbital frontal cortex in response inhibition
(Mega et al., 1997), it is inconsistent with the EEG results showing that increased left
frontal activity is associated with increased aggression and approach behavior (e.g.,
Harmon-Jones & Sigelman, 2001; Harmon-Jones et al., 2003). The interpretation that the
left frontal cortical region is involved in the inhibition of anger and aggression is also
inconsistent with lesion data suggesting that mania results from damage to the right
frontal region (e.g., Robinson & Downhill, 1995) and results obtained when the left
relative to right frontal cortex is activated and angry attentional processes are measured
(e.g., d’Alfonso et al., 2000). However, it is possible that the EEG is assessing
dorsolateral frontal cortical activity and not orbital frontal activity, and that left orbital
frontal activity is involved in the inhibition of anger, whereas left dorsalateral frontal
activity is involved in approach motivations like anger.
In another experiment (Kimbrell et al., 1999), using H2 15O PET, 18 healthy
participants were instructed to recall anxious, angry, or neutral events and then “recall the
emotion they felt during that time and to try to experience it that way again.” (p. 455).
Affect-congruent faces were displayed to participants during the recall “to help subjects
Anger: A review of human electrophysiology 20
re-experience and sustain the emotion.” (p. 455). Compared to the neutral recall task, the
anger recall task evoked increased activity in the left superior temporal gyrus, left inferior
frontal cortex, right thalamus, and right posterior cingulate. Anger also evoked decreased
regional cerebral blood flow in the right superior temporal gyrus, inferior parietal cortex,
and right middle frontal gyrus. However, when anger and anxiety were compared, anger
was associated with greater activity in the brainstem, right medial frontal gyrus, and right
inferior frontal gyrus. Thus, these results suggest that while both anxiety and anger
caused increases in some areas of the left frontal region (as compared to neutral), anger
caused greater activations in some area of the right frontal cortex and brainstem activity
than anxiety. Based on research suggesting that retrieval of personally relevant, time-
specific memories activates the left temporal pole (Maguire et al., 1999), Kimbrell et al.
(1999) suggested “that the common activations by anxiety and anger in the left anterior
temporal and inferior frontal cortical area relate to the nonspecific aspects of recall of
negative emotion…” (p. 461). Clearly, the results of Kimbrell et al. (1999) are
inconsistent with the EEG results reviewed herein and the results of Dougherty et al.
(1999).
As Kimbrell et al. (1999) noted, there were a number of limitations to the
experiment, including the variety of past events recalled and whether the recall task
evoked the actual emotion (the same limitation apply to Dougherty et al., 1999).
Consistent with their concerns about comparing actual emotional experience to imagined
emotional experience, research has demonstrated that moving a thumb activates primary
motor cortex (Rao et al., 1995), whereas imagining moving a thumb activates
supplemental motor cortex (Parsons et al., 1995).
Anger: A review of human electrophysiology 21
Of course, it may be difficult to compare anger induced by imagery to anger
induced by insulting feedback or goal blocking, as in Harmon-Jones and Sigelman (2001)
and Harmon-Jones, Sigelman et al. (2003). In the imagery experiments, there was no
report of a significant association between reported anger and regional brain activity. In
the EEG experiments using means other than imagery to induce anger, self-reported
anger has been found to correlate significantly with relative left frontal activity (Harmon-
Jones & Sigelman, 2001; Harmon-Jones, Sigelman et al., 2003). Examination of
correlations between reported emotion and physiological measures assists in determining
whether the brain activation is related to emotional experience or some other non-
emotional variable.
Comparisons of Violent to Non-Violent Individuals on Frontal Lobe Function
The results indicating that relatively greater left frontal cortical activity is
associated with increased approach-oriented anger and behavior are seemingly
inconsistent with evidence suggesting that violent individuals have reduced frontal lobe
function (e.g., Amen et al., 1996; Raine, Stoddard, Bihrle, & Buchsbaum, 1998; Raine,
Meloy et al., 1998). These results, and others, have led some to conclude that the
prefrontal cortex, particularly the left orbital frontal cortex (and frontal activations
derived from EEG), is involved in the regulation of negative affects like anger (Davidson,
Putnam, & Larson, 2000).
However, other research has more strongly implicated right frontal regions in
violence. For example, Raine, Stoddard et al. (1998) found that murderers who came
from relatively good home backgrounds showed reduced prefrontal functioning,
compared to murderers from relatively bad home backgrounds and normal controls. In
Anger: A review of human electrophysiology 22
particular, the greatest reduction in prefrontal functioning was found in the right
orbitofrontal cortex. Raine, Park et al. (2001) provided further support for this
interpretation in a continuous performance task study that assessed fMRI in violent
offenders. Results indicated that violent offenders who had suffered severe child abuse
evidenced reduced right hemispheric functioning, particularly in the right temporal
cortex. In contrast, individuals who had suffered severe child abuse and had refrained
from violence evidenced relatively lower left but higher right activity in the temporal
lobe. These results suggest that the reduced right temporal activity coupled with severe
child abuse was associated with being violent.
These findings are consistent with the reviewed EEG research (Harmon-Jones &
Allen, 1998; Harmon-Jones et al., 2002; Harmon-Jones et al., 2003), which found that
approach-oriented anger was associated with reduced right frontal activity (in addition to
increased left frontal activity). Other research has revealed that increased activity in the
right frontal cortex is associated with withdrawal motivation. Perhaps the violent
individuals who showed reduced right frontal activity in the studies of Raine and
colleagues (1998, 2001) lack the behavioral constraints engendered by the withdrawal
motivation system that may be partially instantiated in the right frontal cortex.
However, other studies have implicated reduced activity in both left and right
frontal cortices in violence and aggression. For instance, Raine, Meloy et al. (1998) found
in a PET study that affective murderers, as compared to predatory murderers and normal
controls, evidenced reduced lateral and medial prefrontal activity in both hemispheres
during a continuous performance task.
Anger: A review of human electrophysiology 23
Of course, differences in participant samples may explain the differences in
results. That is, most of the anger studies have involved normal individuals, whereas the
studies on violence have involved extremely violent individuals. However, in the
Harmon-Jones and Allen (1998) study, seven of the participants were adolescents who
were in an in-patient psychiatric unit for impulse control disorders. But even among this
sample, trait anger was related to greater left frontal activity and reduced right frontal
activity at rest. These results suggest that the samples may not be the source of the
differences. However, the Harmon-Jones and Allen (1998) samples was much younger
than samples used in other studies comparing frontal lobe function in violent and non-
violent individuals (e.g., Raine, Maloy et al., 1998). The longer lifetime of violence in
adults may cause the reductions in frontal cortical activity.
The studies comparing brain function of violent and non-violent individuals
typically assess frontal lobe function at rest or during a cognitive task and not during
anger-arousing situations. For example, Raine, Maloy et al. (1998) measured PET during
a continuous performance task. However, it is not clear that reduced frontal lobe function
measured during these tasks causes violence. The violent individuals (as compared to the
non-violent individuals) who display less prefrontal activity during cognitive tasks may
simply be less motivationally/emotionally engaged by the relatively unemotional nature
of the tasks. However, violent individuals may not demonstrate reduced frontal lobe
function during a more emotionally engaging situation, such as an interpersonal
provocation. It seems that the brain activation during such events would be more
predictive of violent behavior.
Anger: A review of human electrophysiology 24
Another difficulty emerges when attempting to compare studies of violent
offenders with the studies on anger: anger can be manipulated in the lab, whereas being a
violent offender cannot be manipulated. Thus, in the latter type of studies, there are the
omnipresent difficulties associated with correlational studies. For instance, the violence
may have caused the reduction in frontal activity. Longitudinal studies are needed in
which brain function and violence are measured at several time points, starting in youth
and through adulthood. Such a design would allow researchers to more conclusively infer
whether brain function predicts violence.
In future research on the role of the frontal cortex in anger and violence, it will be
important to distinguish whether the effects of violence on prefrontal activity are due to
anger, impulsivity, or some other variable. In other words, do the causes of the violence
play an important role in the relationship of violence with prefrontal activity?
Importantly, the recent work by Raine and colleagues has begun this type of research as
they have examined differences between affective and predatory murderers, and how
socialization affects relationships between violence and prefrontal activity. Because the
left prefrontal region is supplied with a high density of serotonin type 2 receptors (e.g.,
Mann et al., 1996), and because serotonin has been found to relate to impulsivity (e.g.,
Soloff et al., 2000), it is possible that the reductions in prefrontal activity are due to
impulsivity and not necessarily anger and violence.
Conclusion
In sum, the reviewed experimental research suggests that increased activation of
the left frontal cortical region is associated with approach-oriented anger, whereas
decreased activation of the right frontal cortical region is associated with approach-
Anger: A review of human electrophysiology 25
oriented anger. Evidence also suggests that this pattern of frontal cortical activation is
associated with approach behaviors, some of which can be destructive – aggression
against another person (Harmon-Jones & Sigelman, 2001), and some of which can be
constructive – action taken to resolve a perceived social injustice (Harmon-Jones,
Sigelman et al., 2003). Future research will benefit the understanding of anger by using
brain imaging methodologies with greater spatial resolution to examine neural correlates
of actual outbursts of anger that lead to constructive as well as destructive behaviors.
Moreover, examinations of the neural circuitry of non-violent and violent individuals
during outbursts of anger will assist in understanding one of society’s most destructive
emotions.
Anger: A review of human electrophysiology 26
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Footnotes
1. While there have been several studies examining neural responses to photographs of
angry faces, there have only been a very few studies examining neural activity associated
with the experience or expression of anger. Because the former type of studies are likely
assessing neural processes associated with the perception of emotional stimuli and not
necessarily the experience or expression of emotion, these studies are not reviewed.