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Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

Contents lists available at ScienceDirect

Neuroscience and Biobehavioral Reviews


journal homepage: www.elsevier.com/locate/neubiorev

Review

Human brain EEG indices of emotions: Delineating responses to affective


vocalizations by measuring frontal theta event-related synchronization
Marni Y.V. Bekkedal a, , John Rossi III b , Jaak Panksepp c
a

Two Steps Forward, LLC, 3199 Bookham Dr., Sun Prairie, WI 53590, United States
Department of Social and Behavioral Sciences, Florida Gulf Coast University, 10501 FGCU Blvd South, Fort Myers, FL 33965-6565, United States
c
Department of Veterinary and Comparative Anatomy, College of Veterinary Medicine, Washington State University, Pullman, WA 99164-6520, United States
b

a r t i c l e

i n f o

Article history:
Received 4 September 2010
Received in revised form 23 April 2011
Accepted 3 May 2011
Keywords:
Affective sounds
Emotion
EEG
Alpha blocking
Theta
Gender differences
Auditory perception
Event-related cortical desynchronizations
and synchronizations

a b s t r a c t
At present there is no direct brain measure of basic emotional dynamics from the human brain. EEG provides non-invasive approaches for monitoring brain electrical activity to emotional stimuli. Event-related
desynchronization/synchronization (ERD/ERS) analysis, based on power shifts in specic frequency
bands, has some potential as a method for differentiating responses to basic emotions as measured during
brief presentations of affective stimuli. Although there appears to be fairly consistent theta ERS in frontal
regions of the brain during the earliest phases of processing affective auditory stimuli, the patterns do
not readily distinguish between specic emotions. To date it has not been possible to consistently differentiate brain responses to emotion-specic affective states or stimuli, and some evidence to suggests the
theta ERS more likely measures general arousal processes rather than yielding veridical indices of specic emotional states. Perhaps cortical EEG patterns will never be able to be used to distinguish discrete
emotional states from the surface of the brain. The implications and limitations of such approaches for
understanding human emotions are discussed.
2011 Elsevier Ltd. All rights reserved.

Contents
1.
2.
3.
4.
5.

6.
7.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Electrophysiological correlates of brain affective processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Classications of emotions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Affective communication versus induction of emotion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Measuring affective communication in the brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1.
Spectral power change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Event related potentials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.3.
The ERD/ERS algorithm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Summary of EEG studies and emotions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
ERD methodology and specic emotion evocation methods: from the production, selection and description of stimuli and
experimental procedures to the results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.1.
Production of initial set of stimuli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.2.
Selection of stimuli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.3.
Description of stimuli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.4.
Participants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.5.
Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.6.
Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7.
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7.1.
Changes in emotional states . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7.2.
ERD/ERS analysis: power spectral analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Corresponding author.
E-mail address: 2steps@charter.net (M.Y.V. Bekkedal).
0149-7634/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2011.05.001

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M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

7.7.3.
ERD/ERS analysistheta (3.57/5 Hz) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7.4.
ERD/ERS analysisalpha (812 Hz) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7.5.
ERD/ERS analysisbeta (1330 Hz) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.8.
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Theoretical implications for future work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Implications for the eventual understanding of affective consciousness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
An understanding of the underlying brain dynamics that generate emotional states, especially those that mediate cortical affective
information- and state-processing remains a chaotic area of neuroscience. If one were able to identify emotional feelings and related
cognitive processing of associated stimuli from direct cortical neural recordings, it would have broad implications including the
potential to be applied for improving our approaches for diagnosing and treating neuropsychiatric disorders with symptoms that
include dysfunctional processing of emotional information, such
as autism, depression, mania, and schizophrenia. The aspiration
to perfect such neurometric measures has a long history (e.g.,
John et al., 1988), albeit without any explicit consideration of the
underlying emotional issues.
If we could obtain knowledge about the specicity of EEG
response patterns in the brain related to primary-process emotions, such information may serve as a standard for more accurately
identifying atypical brain activities. The emergence of the eld of
affective neuroscience has opened opportunities for applying scientic rigor and objectivity to the study of the neural substrates
of specic human emotions (Panksepp, 1998), but so far only at
a subcortical level, which is difcult to extend to human studies
except at homologous neurochemical levels (Panksepp, 1986, 1998,
2004). The present paper summarizes the state of the eld from an
affective neuroscience point of view, rather than an informationprocessing cognitive perspective, and summarizes some of our
human EEG work that sought to illuminate such issues.
2. Electrophysiological correlates of brain affective
processes
Basic emotional feelings reect evolutionarily ancient neurodynamics that have yet to be reliably measured from either human
or animal brains. In human research, emotional states are estimated largely from subjective self-reports, and in animals from
ethologically distinct emotional behavior patterns that arise from
neural circuits with distinct affective qualities (Panksepp, 1998).
Part of the problem is that emotional feelings probably reect
large-scale brain network dynamics or emotional action systems
(Panksepp and Bivin, 2011), for which we simply do not yet have
good tools that can directly monitor the relevant subcortical circuit activities (Panksepp, 2000). We do have various impressive
indirect measures, especially fMRI (functional Magnetic Resonance Imaging) and PET (Positron Emission Tomography) that can
estimate energy consumption changes in the brain, albeit those
statistically extracted indirect measures only reect a very small
fraction of ongoing brain activity, with most of it remaining as if
it were background dark energy that does not serve immediate
information-processing capacities, but rather the intrinsic needs of
the brain (Raichle, 2010a,b). It is thought that major problems with
brain functions, as evidenced by various neurological and psychiatric disorders may arise from imbalances of this dark energy of
the brain (Zhang and Raichle, 2010). In any event, such measures
that can identify brain loci that participate in various psycho-

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logical functions do not provide compelling evidence for specic


time-dependent subcortical state-control functions that underlie
emotional feelings, which may be reected in cortical dynamics
to serve various emotional information-processing and regulatory
capacities.
Since it is likely that most psychiatric disorders are characterized by imbalances of brain emotional, and other affective
and affect-regulating systems, it would be good to have direct
brain measures of emotional processing. That has not yet been
achieved. However, by indirectly monitoring the small changes in
energy ripples on the surface of the vast unseen reservoir of brain
energy utilization (called dark-energy by Raichle (2010a,b)), for
instance via fMRI and PET measures, some consistent changes
in neuroanatomically specic arousal patterns for different emotions have been documented. Although some earlier meta-analyses
yielded ambiguous evidence for localization of specic emotions
(Murphy et al., 2003; Phan et al., 2002), new and more sophisticated
meta-analyses, based on 83 studies fullling stricter inclusion criteria, along with voxel by voxel analyses, have documented that the
brain does have clear anatomical signatures for at least ve basic
affective feelings, namely happiness, sadness, anger, fear, and disgust (Vytal and Hamann, 2010). Likewise, clarity has been achieved
about the secondary-processing of affects, namely emotional memory encoding, in various overlapping brain regions (Murty et al.,
2010). Important as that is, such measures of emotionality have
not yet been translated into reliable, psychiatrically useful diagnostic measures, although changes in mid-line resting-state measures
appear to reect rumination, have been useful in distinguishing
depression (see Northoff et al., in this issue). In contrast, we still
have no reliable direct measure of specic neuronal network activities that can distinguish the various basic emotions that arise from
the brain.
3. Classications of emotions
A signicant amount of research into brain correlates of emotion
does not aim to distinguish specic emotions from one another,
but considers them as a generic, more inclusive type of mental
function. The most popular classication is the obvious positive
versus negative affective groupings. Indeed, in early research it was
reported that participants demonstrate a preference to linguistically describe emotions as positive or negative rather than label
them with specic names (Osgood et al., 1957). This classication
has been further promoted through the use of a well-validated set
of visual stimuli from the International Affective Pictures System
(Bradley and Lang, 2007). While there are pictures that represent a
number of different emotions, much of the research that uses the
pictures for generating responses in EEG has focused on positive vs.
negative. While the categories of the valence dimension have been
further delineated based on arousal, there has not been routine use
of the IAPS for differentiating patterns of brain electrical activity
for individual emotions.
Another popular approach reects a broader theory that there
are two opposing behavioral control systems in the brain: the
Behavioral Inhibition System (BIS) and the Behavioral Activation

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

System (BAS) (Bijttebier et al., 2009). Focus on these systems provides a dichotomy for dening emotions based on whether they
are aversive and lead to avoidance behaviors, or are appetitive and
result in approach behaviors. At rst this may appear to simply
be a more rened classication of positive versus negative affect.
However, this perspective considers more than just the emotional
experience but also the corresponding behaviors emitted during
those experiences, as well as overall personality style (Corr, 2004).
While there is some utility in this classication scheme, recent
evidence challenges the clear association of the BIS with negative
emotions and the BAS with positive emotions. The issue centers
on the emotions of fear and anger, both of which have traditionally been classied as negative. While fear seemingly ts with the
categorization of negative emotions associated with activation of
the BIS and resulting defensive behaviors, anger can also involve
appetitive arousal and approach behaviors associated with BAS
activation (Balconi and Mazza, 2009; Carver and Harmon-Jones,
2009). Indeed, EEG response patterns support the later characterization. Balconi and Pozzoli (2009) report changes in activation of
the frontal lobes during pictures of anger that more closely match
what one might expect from activation of the BAS. In the same
report, responses for fear were consistent with those activating the
BIS. Thus, it would seem feasible that although the two emotions
resemble each other on both arousal and valence dimensions, their
activation of underlying behavioral response circuits could result
in differential patterns of activity at the cortical level.
Although there are some studies (e.g., Balconi et al., 2009a,b)
where the research design is conducive to the differentiation of
individual emotions, there is far more research that utilizes the
broader positive/negative categorizations. As such, most studies
include the examination of only three stimulus types: one of
negative affect, one of positive affect, and an emotionally neutral stimulus. Given the paucity of research that makes direct
comparisons within a single affective valence category, the question remains whether or not individual emotions, especially those
revealed by localized subcortical stimulations (Panksepp, 1998)
can be delineated from one another based on neurophysiological
response patterns.

4. Affective communication versus induction of emotion


Approaches used to study the delineation of affective responses
can differ depending on whether the goal is to measure the brain
during a specic emotional state or its response to a stimulus
communicating a specic emotion. Measuring an emotional state
requires the induction of the emotion, and presumably is complicated by the latency of onset for the emotion as well as the
duration of the state. While it will not be the focus here, it bears
noting that EEG changes related to state induction have traditionally been assessed in the alpha frequency band (Davidson, 1992).
Changes in alpha power have been interpreted as indicating differential arousal patterns related to the frontal lobes. A summary of
the work suggests frontal hemispheric lateralization that is based
in the positive versus negative dichotomy, but not in the differentiation of specic emotional states. These patterns have been
most reliably dened as left frontal activation associated with a
positive emotional state and right frontal activation with negative
emotional arousal (Davidson, 1992).
In contrast to measuring changes in emotional feelings, measurement of responses to stimuli that communicate emotions is
simplied by the short latency for response onset, as well as a short
duration of attention to the stimulus. Our interest here is in the
communication of affect and evaluating the instantaneous neurological changes that occur during the instinctual interpretation of
stimuli that convey distinct emotions to the receiver. Stimuli for

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these types of studies have been either visual (Aftanas et al., 2001;
Aftanas et al., 2002; Balconi and Lucchiari, 2006; Balconi and Mazza,
2009; Balconi and Pozzoli, 2009; Balconi et al., 2009a,b; Knyazev
et al., 2008; Knyazev et al., 2009, 2010) or auditory (Paulmann
and Kotz, 2008; Spreckelmeyer et al. (2009). We suspect that the
use of visual stimuli adds an element of irrelevant stimulus complexity that might be minimized with the use of auditory stimuli
such as short human, primate-like vocalizations of various distinct
emotions.
While it is recognized that detection and interpretation of affect
in the human voice is a complex issue (Banse and Scherer, 1996;
Zinken et al., 2008), the use of stimuli with short duration and free
of linguistic content can minimize the non-affective components
of stimuli (i.e., noise) and provide a more pure representation of
emotion. Nonlinguistic components of vocal information play a
signicant role in communicating affective information (Scherer,
1994). Research shows humans can accurately identify emotional
meaning from prosodic features, and this differentiation is for specic emotions, not simply positive versus negative valences, and
not based solely on levels of arousal (Banse and Scherer, 1996).
Thus, such stimuli might be optimal for use in attempts to assess differential brain response patterns during the perception of emotion.
5. Measuring affective communication in the brain
If one aims to monitor brain activity during emotional states and
make comparisons across different states, it is reasonable to employ
measurement tools with relatively low temporal resolution, since
emotions are sustained responses of the brain. In other words, it
is not imperative that immediate responses be measured, or that
assessments involve small (fractions of a second) increments of
time. To assess the brains immediate responses to affective stimuli,
a measurement tool that actually measures neural activity in real
time is desirable, compared to indirect measures as with fMRI and
PET. For routine human research, such instruments are limited to
the electroencephalogram (EEG) and the magnetoencephalogram
(MEG).
The disadvantage of the EEG is its poor spatial resolution at the
cortical level, and the difculty of extrapolating from the cortical activity to what is happening among subcortical processes that
more directly generate affective states. MEG addresses these issues
to some extent, however, it has been used in only a small number
of studies related to the perception of emotion. In two studies using
repetitive transcranial magnetic stimulation to differentiate brain
responses related to prosody, brain responses to two negative emotions (fear and sadness) did not signicantly differ from one another
(Hoekert et al., 2008, 2010). Similar results from a third study (van
Rijn et al., 2005) have been reported, however, response patterns
for sadness and fear differed from those for an emotion of the same
valence (anger) as well as for responses to happiness
In contrast to the small number of studies using MEG, the EEG
has been used much more extensively. Electroencephalography is a
relatively non-invasive approach for measuring brain responses to
discrete stimuli. Although a comparatively old technique for studying brain activity, advances in electronics and computer technology
have allowed increasingly innovative approaches to analyzing
patterns of electrical activity measured in an EEG. Approaches
for evaluating changes in such electrical brain activity fall into
three main categories: (i) overall spectral power changes, (ii)
event-related potentials (ERP), and iii) event-related desynchronizations/synchronizations (ERD/ERS).
5.1. Spectral power change
One traditional approach has been to evaluate the overall power
within a given frequency band under different affect conditions.

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As reviewed in Davidson (1992), alpha is commonly evaluated


for changes related to the induction of different emotions. Overall changes in alpha power, and lateralization effects related to
these changes, as already noted, suggest a relative right frontal
activation is associated with negative emotions, while a relatively
greater left frontal activation is associated with positive emotions.
The effects are limited to categorizing affects as either positive
or negative. In addition to the ndings related to alpha, changes
in the slower theta band have also been found. As reported in
Jausovec et al. (2001), subjects were asked to process emotional
content in lms while their brain activity was monitored. It was
found that changes in theta occurring 23 s into the clip differentiated between subjects with low versus high scores on assessments
of emotional intelligence. Likewise, Andersen et al. (2009), found
the theta band to be especially responsive to anxious ruminative
thinking.
Overall, there are two general problems with simply using traditional spectral power change to measure immediate responses
to affective stimuli. While these studies show differences between
negative and positive emotional valences, patterns that distinguish
between emotions of the same valence have not been consistently
reported. Also, while spectral power changes may be an effective
approach for categorizing brain activity during different emotional
states, it may not be optimal for measuring affective communication responses. Perhaps analytical techniques with greater
temporal resolution are needed.

5.2. Event related potentials


The event related potential is an EEG measure with very high
temporal resolution that allows for the measure of immediate
responses to short stimuli. Traditionally, ERPs are measured as
latencies and amplitudes of positive and negative potentials at
specied millisecond intervals following a stimulus.
Indeed, this approach has been used to evaluate emotional processing in the brain, including responses to prosodic features in
human vocalizations. Paulmann and Kotz (2008) showed results
that suggest the ERP, while able to differentiate affect-related
processing from non-affect-related processing, the ERP components did not differ based on emotional valence. In contrast,
Spreckelmeyer et al. (2009) showed ERP components did differentiate between short vocalizations representing happy and sad
emotions. However, these were the only two emotions tested, and
since they differ on the valence dimension they do not supplement our ability to identify distinct patterns for more discrete
emotions.
Several other studies using ERP measures to assess affective
responses suggest that neural changes within the theta band may
be especially informative. Balconi and Pozzoli (2009) present evidence that the increased theta in response to affective pictures
correlates directly with ERP changes, particularly the N2 component. Furthermore, Kamarajan et al. (2008), reviews evidence to
suggest that some of the ERP changes are a result of underlying
theta increases related to information processing. The changes in
the ERP components and theta increases were a result of participant responses during gains versus losses in a gambling situation.
While it is clear that theta power does change, there are conicting
results as to whether gains or losses are most closely associated
with increased theta (see Kamarajan et al., 2008 vs. Cohen et al.,
2007).
In any event, as with other studies, the ERP data do not show
convincing evidence for patterns of brain activity that readily differentiate between specic emotions. However, it is noteworthy
that some of the ERP components may have a direct correlation
with theta activity.

5.3. The ERD/ERS algorithm


The event-related desynchronization/event-related synchronization algorithm combines the strengths of the spectral power
analysis with those of the ERP analysis. Specically, the ERD/ERS
analysis allows for the evaluation of power changes within specied frequency bands with temporal resolution that rivals the ERP.
As such, it is appropriate for measuring the instinctual reactions to
affective communications as they occur. There are also reasons to
think it holds more promise than traditional ERP measures as they
appear to more closely align along a high versus low arousal continuum and thus may be less able to differentiate between emotions
and better for indicating more general levels of arousal.
ERD/ERS algorithms measure rapid changes of power within
dened frequency band ranges in order to assess responses that
occur within milliseconds of a stimulus presentation. Increased
power within a frequency band following the presentation of a
stimulus is dened as an ERS. ERD refers to a decrease of power in
the specied band following a stimulus. These analyses were rst
introduced by Pfurtscheller and Aranibar (1977) to quantitatively
evaluate changes in the alpha frequency at various cerebral locations under different conditions of mental engagement. Their utility
has since been broadly expanded to include studying concepts
such as verbal comprehension (Pfurtscheller and Klimesch, 1992),
mental planning (Pfurtscheller and Berghold, 1989) and memory
processing (Klimesch et al., 1994).
Additionally, ERD/ERS measures have been assessed, with some
success, for utility in studying emotional responses to affective
communication. Some of the studies have used visual stimuli
(Aftanas et al., 2001, 2002; Balconi et al., 2009a,b; Balconi and
Lucchiari, 2006; Balconi and Pozzoli, 2009) while others have opted
for auditory stimuli including music (Panksepp and Bekkedal, 1997;
Sammler et al., 2007). Although much of the historic ERD/ERS
research, which was generally unrelated to the study of emotions,
focused on the assessment of changes within frequency ranges corresponding to the alpha band, in the range of 812 Hz, more recent
evaluations related to emotion have focused on the slower theta
band (approximately 38 Hz) (Aftanas et al., 2001, 2002; Balconi
et al., 2009a,b; Balconi and Lucchiari, 2006; Balconi and Pozzoli,
2009). Its utility for this purpose is supported by observations that
theta changes distinguish between emotional versus neutral stimuli (Balconi and Pozzoli, 2009; Balconi and Lucchiari, 2006; Knyazev
et al., 2008, 2009), as well as differentiate emotional stimuli based
on their level of reported arousal (Aftanas et al., 2002; Balconi and
Pozzoli, 2009; Balconi and Lucchiari, 2006; Balconi et al., 2009a).
Furthermore, patterns of increased theta power (theta ERS) have
also been shown to differ based on emotional valence as portrayed in visual stimuli (Aftanas et al., 2001; Balconi et al., 2009a,b;
Knyazev et al., 2009, 2010). Results show some of these effects can
be modulated by individual traits such as gender (Knyazev et al.,
2010), alexithymia (Aftanas et al., 2003) and anxious personality
(Aftanas et al., 2003; Knyazev et al., 2008). Furthermore, similar
theta ERSs are noted in other attempts to identify EEG patterns
for emotion including responses to music (Panksepp and Bekkedal,
1997; Sammler et al., 2007) and to lms specically selected for
their emotional content (Jausovec et al., 2001).
The intent of our work in this area was to use the ERD/ERS
analysis as a method for detecting the instinctual brain reactions
that occur during affective communication. It can be used to assess
responses in both implicit or explicit perception paradigms. In
implicit situations, the receiver is more passive and simply experiences the stimuli representing the differing emotions. In an explicit
condition, the receiver is asked to identify the emotion portrayed
in the stimulus. Knyazev et al. (2009, 2010) report timing differences in theta ERS during such implicit versus explicit affective
processing. Results showed that the earliest theta synchroniza-

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

tion occurs in the implicit testing condition, and a later theta ERS
is present during the explicit identication of emotions in pictures of facial expressions. It was proposed that these reect an
unconscious versus conscious processing of the emotion with the
implicit/passive condition being the one of interest for our effort to
identify instinctual affective responses.
Unfortunately, as with other similar efforts using the EEG, this
line of research has failed to clearly demonstrate distinct response
patterns for individual emotions. A commonality between all of
these studies of affect-related ERD/ERS is their universal use of
visual stimuli to communicate emotion. More specically, they
used pictures from the standardized International Affective Picture
System (Center for the Study of Emotion and Attention, 2001), or
pictures of facial expressions from the Ekman and Friesen (1976)
set. As already noted, all visual stimuli tend to have information that
is irrelevant to the emotionality of the pictures used. Thus, we propose that specic emotion-related brain activity changes may be
better detected when the stimuli are presented through the auditory modality. Short, nonlinguistic vocal sounds of emotion may be
less complex than visual portrayals, which require visual scanning
and interpretation of the stimuli, and thus may reduce confounding variables introduced by the more complex cognitive processing
necessary in interpretation of emotional signicance. Furthermore,
evidence suggests there is a difference in a persons accurate classication of an emotion that is dependent on whether the emotion is
communicated in a facial expression versus nonlinguistic vocalization (Hawk et al., 2009). Accordingly, after summarizing additional
EEG approaches to emotion studies, we will proceed to present
results from a project using human vocalizations, that provided an
opportunity to evaluate consistencies in cortical neural response
patterns related to affect independent of confounding sources of
variability as are routinely present in the use of visual sensory input
to the brain.

6. Summary of EEG studies and emotions


In summary, EEG recordings, despite some controversial successes (see Harmon-Jones, 2007), have not yet produced response
patterns sufcient to distinguish brain activity for specic emotions, and thus has failed to provide a tool that could be used to
move forward attempts to apply such techniques to issues of emotional processing changes in psychiatric disorders. Of course there
are abundant general EEG studies in psychiatric patients, including the production of algorithms (e.g., neurometrics) that have
been reported to successfully discriminate different diagnostic categories (Prichep and John, 1992). One of the problems in relating
imbalances in brain emotional processing to psychiatric categories
may be the use of excessively complex stimuli. Indeed, in our EEG
laboratory at Bowling Green State University, we spent years of
fairly frustrating research to see if we could obtain EEG signatures
of basic emotions from cranial EEG recordings of human brains (e.g.,
Panksepp and Bekkedal, 1997) that could potentially be translated
to pre-clinical animal models, where relevant causal analyses could
be done (e.g., see Panksepp, 2000). We largely failed to get good
discriminative signals, perhaps because we initially used complex
emotional stimuli (e.g., music and self-induced emotional motorimagery induced emotional changes). This does not mean that there
were not dramatic changes. There were (see Fig. 1 for one subject
who is an expert at inducing individual emotional feelings as well
as systematically shifting from one to another; please also note that
web access to time dependent changes at narrow alpha ranges are
provided, to highlight how dramatically cortical changes vary as a
function of minor differences in the EEG frequencies analyzed). The
changes, although dramatic, were simply not stable from individual
to individual (partly no doubt because of the use of undergrad-

1963

uate students, perhaps too many with marginal motivations to


follow instructions with a difcult emotion-induction task based
on Manfred Clyness Sentic Cycle approach). But also there were
marginal test-retest reliability patterns in a single subject (data not
summarized here), suggesting that neocortical emotional effects of
idiographic as opposed to nomothetic. In any event, those programs
of research were terminated because of the chaotic nature of the
topographic brain changes observed from subject to subject.
Of course it is also possible that attempts to measure affective impact on the brain as harvested from the cortical surface,
as is typically done in topographic EEG studies, are simply too
far removed from the subcortical emotion generators identied in
animal research (Panksepp, 1998, 2000). While there have been
some encouraging results (Knyazev et al., 2010), to suggest that
certain activity pattern in subcortical regions correlate with distinct activity patterns in the cortex, the evidence is less convincing
with respect to EEG and emotion. However, as noted, there appears
to be an emergence of evidence that suggests the changes in theta
band during the earliest periods of emotion perception are the most
relevant. As such, this may indicate that the cortical theta may be
an extension of theta commonly found in areas of the limbic system
including the amygdala, and most commonly the hippocampus.
Hippocampal (HC) theta has been extensively studied in animal
models of neurobehavioral changes related to emotion and memory. Indeed, Nishitani (2003) used magnetoencephalography to
demonstrate a hippocampal theta ERS in response to negative
and positive emotion pictures with some valence differentiation
related to hemispheric differences. However, a recent, comprehensive review of HC theta research and correlations to cortical theta,
specically frontal midline theta, suggests the absence of any direct
relation between activity in this frequency band at the two different brain levels (Mitchell et al., 2008). Others have proposed a
relation between cortical and HC theta based on the theory that
theta reects a gating mechanism for information that is processed
in the limbic system (reviewed in Knyazev et al., 2010). Even if
this were the case, these authors acknowledge this may mean that
theta analysis could be used to differentiate responses to emotional
versus neutral stimuli, although it may hold minimal promise for
distinguishing between emotions.
Unfortunately substantive data to address the relationship of
waking subcortical theta changes to the corresponding theta at the
cortical level are not yet available, although it has been proposed
that theta in the limbic system directly correlates with theta oscillations in the frontal cortex, and thus is likely to be involved in some
regulatory component of affective states and neurobehavioral proles (Miller, 1991; Knyazev, 2007). As previously reviewed, there
seems to be ample evidence to suggest that in emotion studies,
increased cortical theta power does not differentiate much more
than a simple dichotomy of emotional versus psychologically neutral states, with data suggesting that theta ERS is greatest for stimuli
of negative valence, somewhat less for positively valenced stimuli,
and least for emotionally neutral ones.
Still, it is possible that discrete emotions can be distinguished
at the subcortical level, but the cortical correlates of those primal
emotional responses are not typically veridically reected in cortical activity (Panksepp, 2000). At present, considerable obstacles
remain studying brain EEG responses as they relate to discrete
human emotions and affective communications. A major impediment currently is unavailability of tools that allow investigators
to employ very clean emotional stimuli and to deploy such stimuli
with concurrent direct monitoring of brain activity changes with
sufciently high temporal and spatial resolutions. Of course, the
EEG remains the tool of choice with regard to real-time recording
of human neural activities, but adequate temporal resolution may
be imperative for measuring brain emotional changes that reect
distinct affect arising from discrete instinctual-emotional response

1964

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

Fig. 1. Cortical regional differences in EEG alpha power shifts (within the full 813 Hz range) monitored from the cranial surface of one subject (Jaak Panksepp) during the rst
4 s periods after successive emotional inductions using Clyness Sentic Cycles procedure (see Clynes (1977) as well as Panksepp and Clynes (1998)). Each emotional dynamic
was repeated 20 times, using the timing recommendations for the Sentic Cycles exercise. The sequence of emotions, was left to right: (i) neutral expression, (ii) anger, (iii)
sadness, (iv) love/lust, (v) joy and (vi) reverence. Four successive 1-s epochs (top to bottom) are depicted following initiation of the experiential emotional dynamic, assisted
by bilateral mild dynamic pressure between index nger and thumb, in seated meditative position. A successive quarter second analysis (as a pseudo-video) of each 4 s period,
broken down into 2 Hz analysis is available on the web site provide below. It was remarkable how dramatically power shifts in these fractional alpha-frequency ranges differed
from each other, highlighting the complexity that has to be faced when doing such analyzes (see http://www.vetmed.wsu.edu/research vcapp/Panksepp-endowed.aspx).

systems (Panksepp, 2000). Yet, the EEG has relatively poor spatial
resolution at the cortical level for picking up discrete network activities, and at best, one can only infer localized subcortical activity
changes, even though that is where most of the affective action
may be occurring (Panksepp, 1998).
Obviously, electrical brain activity measurement at the subcortical level is invasive, and thus not practical for routine human
research. It is possible to attempt parallel types of investigations
using simultaneous cortical and subcortical recordings in animal
models, however, the ability to clearly delineate discrete emotional
stimuli, affective states and corresponding emotional responses in
these models, in time-locked ways, remains a challenge. We do suspect that the use of emotional vocalizations, as in the experiment to
be described, is the optimal way to proceed, since the same methods
could be used in both human and animal research. In anticipation
of such possibilities, in the following experiment we attempted to
rst apply this strategy to the human brain, to determine if distinct
emotion-specic signatures of brain changes could be obtained
that could then be translated to animal models for ner analyses.
Of course, other brain imaging techniques, such as the fMRI
and PET, have much greater spatial resolution and allow for the
visualization of simultaneous activity throughout the entire brain.
However, their relatively poor temporal resolution makes them
less ideal as a tool for measuring the rapid onset, short duration
responses to affective communications. Additionally, their routine
use in cross-species affective neuroscience research is not yet readily available.
Before conceding to the possibility that the EEG cannot be used
to delineate various discrete primary-process emotional responses,
we proceeded to design the simplest possible experiment we could

imagine that may have efcacy in cross-species follow-up research.


We aimed to use what we thought would be the most robust emotional stimuli we could ethically use, namely the raw emotional
intonations of the human voice (see Zinken et al., 2008).
Accordingly, we selected a classical dimensional approach,
where affective space was split into positive and negative sectors, along with high and low arousal quadrants. The intent was
to create a scenario that would allow for the evaluation of differences that could distinguish within and across valences, as well
as delineate effects that appeared to be more based in generalized levels of arousal. The stimuli were raw (single exhalation)
sounds of four primal feelings: (i) anger (negative valence, high
arousal), (ii) joy (positive valence, high arousal), (iii) sadness (negative valance, low arousal) and (iv) pleasure (positive valence, low
arousal). We created a library of stimuli generated by an emotionally sophisticated set of volunteers, and the validity of their
affective content was insured by only selecting stimuli that a separate group of receivers identied correctly with close to 100%
accuracy. These stimuli were used in the following topographic EEG
recording experiment to see if we could also identify four distinct
affective states through a sophisticated analysis of cortical neurodynamics using topographic EEG ERD/ERS recordings as the direct
measure of ongoing neurodynamics.
In the following sections we will describe the measurement
of changes in cortical electrical responses to nonverbal human
vocalizations representing joy, pleasure, sadness or anger. When
combined with information from related measures, such as personality scales that attempt to monitor primary-process emotional
strengths and weaknesses (e.g., Davis et al., 2003), the results may
contribute to the development of a common reference point from

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

which to identify typical versus atypical affective response patterns


of the brain.
7. ERD methodology and specic emotion evocation
methods: from the production, selection and description of
stimuli and experimental procedures to the results

1965

on a scale from 0 to 10. Some reliable differences were found in


the intensity ratings for the emotion-related sounds, and a main
effect for emotion (p < .0005) was found where joy and anger were
rated as more intense (7.3 0.3 and 8.0 0.2, respectively) than the
pleasure or sad stimuli (6.5 0.3 and 6.6 0.4, respectively).
7.5. Procedures

7.1. Production of initial set of stimuli


Eight adult male (n = 5) and female (n = 3) performers provided
the initial set of affective vocalizations. During a recording session,
each performer was instructed to emit one individual vocalization
representing their interpretation of the emotions of joy, pleasure,
anger, sadness, excitement, love, disgust and fear. Each performer
provided one sound for each emotion for a total of 64 sounds. During the recording session, the sounds were digitally recorded into
a computer (16-bit, 44.1 kHz). They were transferred, in random
order, to digital audio tape (DAT) for presentation to a group of
independent raters.
7.2. Selection of stimuli
Twelve individual raters were given a list of the eight options
for emotion type and a rating sheet that provided space to identify
the emotion type for each sound, and separate scales for rating the
valence and intensity of each sound. Each of the 64 sounds was
played with sufcient time between each sound to allow for rating
scales to be completed. The goal was a nal set of sounds tting into
four groups: positive high intensity, positive low intensity, negative
high intensity and negative low intensity. Results from the rating
exercise identied joy sounds as positive high intensity, pleasure as
positive low intensity, anger as negative high intensity and sadness
as negative low intensity. For each of these four emotion types, the
ve vocalizations with the highest rate of agreement were selected
for a nal experimental set of 20 sounds (ve sounds from different
emitters for each of the four emotion types).
7.3. Description of stimuli
Stimuli presented to subjects during the EEG recording were
ve sounds for each of the four selected emotion types: joy, pleasure, anger and sadness. The average (SEM) intensity rating (0 = no
intensity, 6 = high intensity) for each of these groups was 4.0 0.2
for joy, 3.5 0.2 for pleasure, 4.9 0.2 for anger and 3.4 0.2 for
sadness. Each of the ve sounds in an emotion group was different and thus had slightly different durations. The average duration
for each stimulus subset was 690 69 ms for joy, 977 96 ms for
pleasure, 865 66 ms for anger and 968 80 ms for sadness. Only
joy was signicantly different from the others and we deem this
to be a potentially interesting ethological nding for human emotional vocalizations. The emotionally neutral stimuli were a set of
ve pure tones at 500 Hz, 750 Hz, 1000 Hz, 1500 Hz and 2000 Hz, all
with a duration of 1000 ms.
7.4. Participants
Eleven adult males and eleven adult females were recruited for
EEG recording. Data from one male participant were eliminated due
to excessive muscle artifact apparent in the EEG recording. Each
person was tested at least 2 h after their last meal and at least 24 h
following the last intake of caffeine.
To reduce the effects of stimulus novelty, all subjects were asked
to listen to and rate each sound in the collection of emotion-related
vocalizations during a habituation/pre-testing session on the day
prior to EEG recording. Specically, subjects were asked to identify the emotion represented in each sound and rate its intensity

The subjects were tted with a standard recording cap (ElectroCap International) with 19 electrodes systematically placed
according to the 10/20 system (Jasper, 1958) with linked earlobes
as the reference. Each electrode was lled with electrically conductive gel (Electro-gel, Electro-Cap International), and the scalp was
abraded until impedances at each electrode were <10 k. Subjects
were tted with a pair of monaural headphones placed over the cap,
and were seated in a comfortable chair located inside a dimly lit,
sound-attenuated audiology testing booth. They were instructed to
remain seated with eyes closed and relax in order to minimize the
effects of muscle movement.
Each session began with 3 min of silence for a baseline recording,
followed by the presentation of ve different pure tones repeated
45 times each throughout the next 3 min with an interstimulus
interval of 10 s. Then one group of emotion sounds was presented
such that each of the ve different vocalizations for that emotion set
was presented 45 times during the next 3 min with an interstimulus interval of 10 s. This was followed by another 2 min presentation
of the pure tones. Following the second pure tone set, data recording was paused while the subject was asked to verbally label the
emotion represented in the majority of the most recent presentation of vocalizations, and provide an average intensity rating for
those sounds. This pattern of presentation was repeated for the
remaining three emotion subsets. The order of emotion subsets was
arbitrarily chosen for each subject such that a set of positive vocalizations was always followed by a subset of negative vocalizations
or vice versa. Following the recording session, subjects were asked
to describe any changes in their emotions that may have occurred
during testing by identifying the emotion experienced and rating its
intensity. These questions were meant to determine if the sounds
evoked a lasting change in the participants emotional state.
7.6. Data analysis
Muscle artifacts in the EEG records were manually identied and
removed from further analysis. Data were further reduced with a
150 Hz lter to eliminate all frequencies outside of that range.
The data were Fast Fourier transformed, and power spectra were
calculated for each of the 3 min presentations of different emotionrelated stimuli. Values were obtained for theta (3.57.5 Hz), alpha
(812 Hz) and beta (1330 Hz). Second, ERD/ERS analysis was
employed to determine stimulus-related changes in the power of
the same three frequency ranges. The percent change in each frequency band was calculated as (R A/R) 100), where R and A are
the EEG power of the specied frequency in the reference and test
intervals, respectively (Pfurtscheller and Aranibar, 1977). In this
study, the reference interval was identied as occurring 1 s prior to
the stimulus onset and the test intervals 01 s from the onset of the
stimulus. The averaging sweep was 0.5 s such that the test interval
was divided into two equal time increments, 00.5 s and 0.51 s. As
nearly all responses had returned to baseline by the 0.51 s interval,
only the rst epoch (00.5 s) was included for further analysis.
For the purpose of a global analysis, data from individual electrodes were averaged together such that the scalp was divided into
quadrants and three electrodes from each quadrant were averaged.
Specically, scores for the right anterior quadrant included the Fp2,
F4 and F8 electrode sites. Sites Fp1, F3 and F7 were used for the left
anterior. Electrodes P4, T6 and O2 made up the right posterior and

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

% of Reference Theta
Power

120
110
100
90

% of Reference Theta
Power

Anterior Left

130

Neutral

Joy

Pleasure Anger
Emotion Type

130
Posterior Left
120
110
100
90

Neutral

Joy

Pleasure Anger
Emotion Type

Sad

Anterior Right

130
120
110
100
90

Sad

% of Reference Theta
Power

% of Reference Theta
Power

1966

Neutral

Joy

Pleasure Anger
Emotion Type

Sad

130
Posterior Right
120
110
100
90

Neutral

Joy

Pleasure Anger
Emotion Type

Sad

Fig. 2. Changes in theta power based on percent of baseline power in response to different stimuli. Results are averaged across electrodes on each of four quadrants of the
scalp. The gure demonstrates the greatest theta synchronization in the anterior hemisphere and in response to sounds of anger and pleasure. Filled bars are for males and
open bars are for females.

7.7.1. Changes in emotional states


Very few subjects reported any lasting change in emotional
state, and those that did reported minimal changes (intensity ratings <2). The data suggest there was not a lasting shift in the
subjects affective states during any of the different sound types
and changes in brain activity were more related to the instant perception of the stimuli.
7.7.2. ERD/ERS analysis: power spectral analysis
Greater alpha and less beta power in the anterior regions of the
brain as compared to posterior regions (p < .0001) was observed
across all stimulus types. No overall regional differences were found
for the theta band. No overall changes in theta, alpha or beta power
were found in relation to the different emotional sounds.
7.7.3. ERD/ERS analysistheta (3.57/5 Hz)
A complex 3-way interaction of gender emotion brain
region was found (p < .05). All differences relating to gender and
emotion occurred in the anterior regions of the brain rather than
the posterior ones (Fig. 2).
The most robust difference between the males and females was
in response to the anger sounds (p < .05) where females demonstrated a greater increase in theta than did males. This difference
was apparent in both left and right anterior regions (ps < .05), but
was not found in the posterior regions. A gender difference was
also found for responses to pleasure sounds (p < .05) where females

% of Reference Theta
Power

7.7. Results

showed less of a theta power increase than males. This effect was
statistically reliable in the right anterior region only.
Some differences were found in response to emotional sounds
within genders (Fig. 3). In males, moderated ERDs occurred during
joy and anger sounds. This change was signicantly different form
the ERS observed during pleasure sounds (ps < .05). Responses to
neutral sounds were modest ERSs that did not differ from responses
to any of the other sounds. In females, all responses were theta
ERSs. The ERSs for joy and pleasure were reliable smaller than
those observed during anger sounds (ps < .05). As in males, female
responses to neutral and sad sounds did not reliable differ from the
brain changes during the other emotional sounds.
A 2-way interaction was found for brain regions time
(ps < .0001) where theta power increased in the 0.00.5 epoch

% of Reference Theta
Power

P3, T5 and P1 were the left posterior. There were no signicant


differences between individual electrodes within a quadrant. Data
from Fz, Cz, Pz, T3, T4, C3 and C4 were not included in the nal
analyses.
For each of the three frequency bands, the percent change
in power was averaged and subjected to a ve factor, repeated
measures ANOVA: gender (2) stimulus type (5) brain quadrant
(4) electrode (3) time interval (2). This was done for both the
power spectra and the ERD/ERS analysis, although the ANOVA for
the power spectra did not include the time interval variable.

115

Males

110
105
100
95
Neutral

Joy

90

Pleasure

Anger

Sad

Anger

Sad

Emotion Type

115

Females

110
105
100
95
Neutral
90

Joy

Pleasure

Emotion Type

Fig. 3. Gender differences in changes of theta power based on percent of baseline


power. Changes are in response to sounds of different emotion types. The gure
demonstrates gender differences in response to anger and pleasure.

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

and decreased in the 0.51.0 epoch. This pattern was the same
in all brain regions, however, the magnitude of the changes was
greater in the anterior regions in comparison to the posterior ones
(p < .005). These differences were not observed during the 0.51.0
epoch. The statistical main effect for time (p < .0001) was due to
an increase in theta during the 0.005 interval (112.3 0.6%)
and a subsequent decrease during the 0.51.0 interval
(95.2 0.8%).
7.7.4. ERD/ERS analysisalpha (812 Hz)
Changes in the alpha band did not differentiate the emotional
stimuli. This is important, for alpha-blocking (i.e., ERD) types of
experiments have been typically successful using cognitive, nonemotional stimuli (see especially the cited work by Wolfgang
Klimeschs group). Still, some small effects were also observed
here. Modest differences were observed between the anterior and
posterior regions of the brain, where overall there were greater
reductions in alpha power in the posterior regions than the anterior
ones [brain region time (p < .05)]. Differences were found during
the 00.5 epoch where alpha desynchronization was less in the
left anterior region than in either the left or right posterior regions
(ps < .05). During this epoch, the decrease in alpha was less in the
right anterior region than the left (p < .05), but was not different
from the right posterior region (p < .10). There were no regional differences during the second half of the recording interval (0.51.0).
7.7.5. ERD/ERS analysisbeta (1330 Hz)
Similar to changes in the alpha band, response patterns in
the beta wavelength did not distinguish between the emotional
stimuli. No signicant left-right hemispheric differences were
found for either the anterior or posterior regions. A main effect
for brain regions was observed, reected by slight decreases in
beta power in the left and right anterior regions (99.7 0.6% and
99.5 0.5%, respectively) accompanied by modest increases of
beta power in the left and right posterior regions (101.8 0.5%
and 100.9 0.4%, respectively). The differences were statistically
reliable only between the left and right anterior regions and left
posterior region (ps < .01)
7.8. Discussion
The present experiment evaluated the use of ERD/ERS analysis in
differentiation of brain responses to nonlinguistic vocalizations of
joy, pleasure, anger and sadness. This expanded previous research
that has traditionally used visual stimuli including images of emotional situations (Aftanas et al., 2001, 2002) and pictures of affective
facial expressions (Balconi and Lucchiari, 2006). The results provided limited support for our hope that theta ERS patterns would
differentiate responses to distinct emotion-related sounds. The
results were consistent with previous research where the most
salient effects were observed in theta ERSs in anterior regions of the
brain (Aftanas et al., 2001, 2002; Balconi and Lucchiari, 2006). However, in prior studies these changes were not dependent on emotion
type but rather were more generically related to emotion versus
non-emotion related stimuli. Even so, an unanticipated and novel
nding of gender differences was observed that was based on the
differentiation of responses related to specic emotions. It may be
an important consideration for future research to carefully evaluate gender-specic responses. It may also be valuable to categorize
stimuli based on specic emotions as opposed to broader categorizations of neutral versus emotion-related (Balconi and Lucchiari,
2006), positive versus negative valence (Aftanas et al., 2001) or
differentiation based solely on the rated arousal levels of the emotional stimulus (Aftanas et al., 2002).
In females, the anger stimuli provoked the largest EEG
response. This is consistent with a previous report where women

1967

viewing lm clips showed greatest theta increases during segments with strong aggression-related content as compared to an
emotionally neutral clip or segment portraying sadness (Krause
et al., 2000). Additionally, functional magnetic resonance imaging
changes show that womens brain activation patterns in response
to facial expressions of anger versus fear are more discriminating than responses in men. This gender difference is not apparent
in adolescence suggesting a culturally learned effect where adult
women have learned to attend to indications of anger and a
potentially threatening situation, and corresponding emotional
stimuli cause a characteristic defensive response (McClure et al.,
2004).
Although theta ERS does correlate with the appraisal of the
emotion-related sounds, the psychological corollary of theta activity remains unclear. Previous ndings related to theta ERS suggest
its relationship to working memory (see reviews by Klimesch,
1996; Klimesch et al., 1996) and episodic memory (Doppelmayr
et al., 1998; Klimesch et al., 1994, 1997a,b). Last, overall theta
power in the frontal regions of the brain is directly related to
the amplitude of evoked potential response in the same areas
(Basar et al., 1998). Greater evoked potentials are traditionally
interpreted as elevated levels of attention directed towards a
specic stimulus. Such evidence may suggest the theta differences
during emotional sounds, as found here between women and men,
may reect differences in allocation of attention. However, it is
not possible from the present data to determine conclusively that
women paid more attention to the anger sounds than to others or
gave them more attention than males did.
While it is possible women were more psychologically alerted
by the sounds of anger than the men were, it seems unlikely the
differences occurred because they were more distressed or experienced some other more lasting change in their emotional state.
Theta ERS was consistently found during the earliest part of the
stimulus presentation (rst half second), but had returned virtually to baseline by the next half second. Presumably a more global
change related to variations in emotional states would have lasted
longer than this fraction of a second. Also, there did not appear
to be any residual effects from the sounds since there were no
general changes in the overall power spectra across the stimulus
types for any of the frequency bands evaluated. Thus, results from
the spectral power analyses suggest a relatively constant baseline
state of brain activity, and likely a constant affective state in the
test subjects.
Although the results show consistent theta ERSs, there are only
modest differences between responses related to different discrete emotional sounds used, and in some cases changes related
to neutral tones were equal to or greater in magnitude than
changes during emotional vocalizations. It is possible that such
changes reect the commonly observed see-saw dynamics of cortical and subcortical activities seen in human brain imaging (Liotti
and Panksepp, 2004). As such, it does not appear that theta ERS
changes are sufciently sensitive to delineate distinct brain activity responses related to stimuli representing different emotions.
However, these data, combined with those from research evaluating visual depictions of emotion, suggest theta ERS may be a more
sensitive marker for the arousing qualities of emotional stimuli and
less differentiating for emotional valence. In conclusion, although
theta ERS patterns consistently appear in response to emotionrelated stimuli, they are insufcient for clearly dening typical from
atypical response patterns.

8. Theoretical implications for future work


Is it possible to ever get a clean EEG signal from surface recordings that might highlight the neurodynamics of basic emotional

1968

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

processes in the brain? We suspect that may not be possible,


perhaps largely because the higher reaches of the human brain are
largely programmed by life experiences, and different emotional
neurodynamics in different people are idiosyncratically related to
higher-cognitive brain functions (see Fig. 1 legend). And we say
this with full consideration of the fact that emotional specicity is
evident in subcortical brain regions of all mammals that have been
studied (Panksepp, 1998) and a recent fMRI and PET meta-analysis
of evidence for basic emotions found very robust evidence for
distinct brain metabolism/blood-ow signal changes so that every
one of the following emotions could be distinguished from each
other happiness, sadness, anger, fear and disgust (Vytal and
Hamann, 2010). Those results are impressive, but practically all
the hot-spots were fairly deep in the brain, in either subcortical
structures, or limbic cortical regions, and practically none were
represented just adjacent to 10/20 cranial recording sites traditionally used in human EEG studies. Further, it is possible that the
medial frontal cingulate and temporal regions implicated in that
meta-analysis are already high enough in the brain to be mediating
the cognitive thought-related aspects of emotions rather than the
primal feeling states.
However, there are excellent studies that specically attempted
to monitor basic emotional-affective feelings with PET (e.g.,
Damasio et al., 2000), which found arousals almost exclusively in
subcortical brain regions that have been identied as part of the
primary-process emotional networks in all animal brains that have
been studied with brain stimulation procedures (for summary, see
Fig. 4).
The reasons emotion-specic anatomies are not evident in cortical EEG studies is, as already noted, due to the simple fact that
essentially all cranial sites used in 10/20 recording arrays are far
removed from the primary generators of the various basis emotions, and hence there is little chance for clear emotional signals to
be evident at the neocortical surfaces (for more discussion of these
points, see Panksepp, 2000). This may preclude the possibility that
studies such as this will ever get clear surface EEG indicators of basic
affective processes. However, this should not be taken to mean that
more renement of neurometric procedures may not eventually
be able to provide robust diagnostics of brain-psychiatric problems that are characterized by poor emotion regulation (e.g., John
et al., 1988). Cortical EEG measure may simply not be adequate to
probe the depths of the subcortical affective mind, except perhaps
in pre-clinical mammalian models where well-situated recording
sites can more directly harvest neural eld potentials from brain
networks that generate primary-process emotionality.
Directions for future research may include measuring theta
for similar emotions presented via different modalities. It will be
important to know if facial expressions of happiness correlate
highly with those measured during happy vocalizations. Future
research also needs to focus on including more than a single
emotion within the same valence to ensure observed differences
between emotions are not simply related to valence, but rather
are specic to that emotion. There is research to suggest that nonverbal vocalizations and facial expressions of emotions generate
the greatest accuracy for identifying the represented emotion as
compared to accurate interpretations of speech embedded prosody
(Hawk et al., 2009). By using modalities and stimulus-types where
accuracy is not an issue, the neurophysiological correlates could
be the primary focus. However, attempts to utilize EEG measures to monitor specic emotions has barely been developed,
and if successful, such measures could be especially useful for
addressing the needs of people with neuroaffective disorders.
With modern new computational techniques that yield easy to
interpret heat-maps of EEG changes (e.g., Gordon, 2011) this
approach may yet succeed where more traditional procedures
have not.

Fig. 4. Relative patterns of cortical and subcortical arousals and inhibitions in


Damasio et al.s (2000) imaging of four primal human affects, 189 brain sites exhibited signicant changes in blood ow. The top half of the graph indicates the
percentage of sites of those exhibiting arousals that were located in neocortical
areas vs. those that were situated in subcortical brain regions. The bottom of the
graph indicate comparative percentages for the brain areas that exhibited reductions in blood ow. Clearly, neocortical areas tended to exhibit decreases in arousal
for each of the emotions, while those below the neocortex tended to exhibit the preponderance of increases. Overall, sadness and anger had the biggest effects on the
human brain while happiness and fear had smaller overall effects. However, please
note that anger had the largest relative arousal effects on the neocortex, which may
suggest the largest invigoration of cognitive activities.

9. Implications for the eventual understanding of affective


consciousness
Part of our interest in EEG measures was based on the likelihood that such approaches might yield the rst global insights
to the wide-scale network dynamics, synchronizing among many
brain areas (Singer, 2009), that constitutes affective consciousness
(Panksepp, 2007). That was not achieved, although a hint of what
might eventually be obtained was evident (e.g., Fig. 1). Of course
the neural correlates of consciousness have been studied for some
time, but what is most critically important is to specify the constitutive processes (i.e., in other words, the causal infrastructure)
of consciousness (Neisser, 2011), especially the most ancient phenomenal forms which we suspect are experientially affective in
nature (Panksepp, 1998).
Considering the well-established fact that the foundations of
consciousness are subcortical (for review, see Watt and Pincus,
2004) this will require monitoring of global neurodynamics, where
EEG measures are still the only direct measures of neural activity that we have, that can be applied in very similar, nonverbal
ways in both humans and animals. We still think such cross species
studies of emotional vocalizations, along with studies of subcortical emotional networks (Panksepp, 1998) are the most promising
cross-species avenue for further investigations.

M.Y.V. Bekkedal et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 19591970

Because of the bipolar affective structure of raw emotional


feelings, namely various negative and positive affects, raw emotional feelings may be an ideal way to make scientic progress
on the neural nature of consciousness, and hence the fundamental sources of mind in brain evolution. We already know that
wherever in the brain one applies highly localized electrical and
chemical stimulation and obtains coherent emotional behavior patterns, animals will treat these within-brain, articially induced
arousals as rewards and punishments in various learning tasks
(Panksepp, 1998; Panksepp and Bivin, 2011). Likewise, humans
consistently report experienced affective changes to such articial
brain arousals (early work summarized in Panksepp, 1985, and see
Coenen et al., in this issue). These highly replicable effects can currently be deemed gold standards for the existence of affective qualia
in animal and human brains.
Such models provide distinct methodological advantages
for empirically decoding the neural nature of phenomenalaffective consciousness, namely the raw emotional experiences
(i.e., affective qualia). A Powerpoint pseudo-video example of our attempts to do this in humans using cortical
EEG measures are available at the following web-site
(http://www.vetmed.wsu.edu/research vcapp/Pankseppendowed.aspx). A progressive epistemology for understanding the
primal nature of the affective mind might be as follows:
(i) Identication of brain sites across several species of mammals
that evoke such hedonic effects (using various types of direct
brain stimulation including modern optogenetic approaches).
(ii) Identication of the major additional brain regions that are
most strongly impacted by such brain arousals (e.g., via cFos
histochemistry, etc.).
(iii) Harvesting the uctuating neurodynamic correlates from these
same primary-process brain regions (as with quantitative highdensity cortical EEG in humans during experimentally induced
affective states, supplemented by relevant subcortical site
recording in animal models) as a function of intensity and
duration parameters of relevant brain stimulations, while monitoring affective and behavioral changes. This would allow
estimation of the global neurodynamics that instantiate affective mind in brain activities.
(iv) Identication of key chemistries that modifyi.e., attenuate
and intensifythe above effects in animals and humans, and
monitor the above shifts in brain dynamics.
(v) And nally, provide additional testable predictions, genetic
and otherwise, from the above ndings (especially with
respect to ethically/therapeutically acceptable neural intervention strategies for various mental problems), for instance
anxiety, depressive and manic states, to help validate the productiveness of the preclinical evidence.
In sum, this program of research namely, a technological
extension of a standard cross-species affective neuroscience strategy can be pursued in other animals because of the existing
robust behavioral indices of the bipolarity of affective neural
circuits in many other mammals (i.e., the reward and punishment effects of specic network activations), which correspond
well with more modest work that has already been conducted
in humans. Abundant empirical indications currently converge
on the conclusion that subcortical neural networks sufce for
the generation of primary-process affective processes, making
animal-models potentially highly efcacious for deciphering the
underlying cross-species neural principles in ways that can be
translated to human research, with predictions that can conrm/support or disconrm/negate specic aspects as well as
the overall theoretical supra-structure. In such work, it will be
especially important that one can provoke deep primary-process

1969

emotional states in animals both on the input side, as with emotional vocalizations, and on the output side using appropriate
subcortical stimulations. This type of strategy may be able to reveal
the causal/constitutive primary-process infrastructure of human
and other mammalian minds, which may progressively lead to
similar probing of the more diverse, higher-order evolutionarily
emergent levels of cognitive mental processes that take hold mostly
through experience-dependent cortical maturation, and perhaps
partly through higher neural evolutionary functions that currently
remain largely unknown. If the dynamic signatures of emotionally felt states of mind could be empirically measured, we expect
that it would lead to a better understanding of our deep affective
nature, which may be fundamental for understanding psychiatric
disorders.

Acknowledgements
Funding for this research was provided to the Department of
Psychology, Bowling Green State University, Bowling Green, OH
43403, USA from the Ofce of Naval Research (F3360197MT040) to
JR. During the construction of this manuscript, J.P. was supported
by funding by the Hope for Depression Research Foundation.

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