Models of brain asymmetry in emotional processing

Abstract

Two models of brain asymmetry in emotional processing were reviewed: the right hemisphere and the valence hypotheses. The first states a dominant role for the right hemisphere in emotional processing, whereas the second assumes that the left hemisphere is dominant
for positive emotions and the right hemisphere for negative ones. Different methods, such as the divided visual field technique, have
supported both hypotheses. The amygdala and the prefrontal cortex are presented as important structures involved on brain asymmetry
in emotional processing. The paper ends pointing out new perspectives for the study of the neural subtrates of different components of emotions. Keywords: brain asymmetry, right hemisphere hypothesis, valence hypothesis.

Full text

Models of brain asymmetry in emotional processing
Nelson Torro Alves1, Sérgio S. Fukusima1 and J. Antonio Aznar-Casanova2
1 Universidade de São Paulo, Ribeirão Preto, Brasil
2 Universidad de Barcelona, Spain
Abstract
Two models of brain asymmetry in emotional processing were reviewed: the right hemisphere and the valence hypotheses. The rst
states a dominant role for the right hemisphere in emotional processing, whereas the second assumes that the left hemisphere is dominant
for positive emotions and the right hemisphere for negative ones. Different methods, such as the divided visual eld technique, have
supported both hypotheses. The amygdala and the prefrontal cortex are presented as important structures involved on brain asymmetry
in emotional processing. The paper ends pointing out new perspectives for the study of the neural subtrates of different components of
emotions. Keywords: brain asymmetry, right hemisphere hypothesis, valence hypothesis.
Introduction
Despite the new insights provided by several behavioral,
neurological and lesion studies (e.g., Sackeim et al., 1982;
Adolphs, 2002; Rodway, Wright, & Hardie, 2003), the exact
role of cortical asymmetries in the emotional processing
remains unclear. Currently, two different models on the
processing of emotions and facial expressions have received
considerable attention: the right hemisphere and the valence
hypotheses, which have been supported by a great number of
studies (Ley & Bryden, 1979; Davidson, 1983; Borod et al.,
1998; Asthana & Mandal, 2001; Jansari, Tranel, & Adolphs,
2002; Tamietto, Corazzini, Gelder, & Geminiani, 2006).
The purpose of this paper is to present these two models
which propose an asymmetry in emotion processing.
The divided visual eld paradigm is described and the
participation of the amygdala and the prefrontal cortex are
discussed. The review ends pointing out new perspectives
for the study of brain asymmetry.
The right hemisphere hypothesis
The oldest theory about brain asymmetry states that
the left hemisphere is associated with cognitive processes,
whereas the right hemisphere is involved with the processing
of emotion. The association between emotion and the right
hemisphere appeared very early in the neurological literature.
In 1912, Mills observed that damage to the right side of
the head caused a decrease of the emotional expression.
Similarly, Babinski (1914) veried that patients with lesions
in the right hemisphere became manic or emotionally
indifferent. Those initial studies led to the development of
the right hemisphere hypothesis, which states a dominant
role for the right hemisphere in the processing of all
emotional components (Borod et al., 1998).
Many studies have provided support for this hypothesis.
For example, Sackeim, Gur and Saucy (1978) found that
facial expressions are more intensely expressed in the left
side of the face, suggesting a greater involvement of the
right hemisphere in the production of emotional displays.
Adolphs, Damasio, Tranel and Damasio (1996) veried that
patients with right hemisphere damage were more impaired
in recognizing facial expressions than patients with left
hemisphere damage. Some authors have also suggested
that the right hemisphere might contain a store of structural
representations or templates of facial expressions (Blonder,
Bowers, & Heilman, 1991; Bowers, Blonder, Feinberg, &
Heilman, 1991). Once these templates are destroyed, by
a stroke or cerebral injury for example, the capacity to
recognize facial expressions could be lost.
The negative / positive and the approach /
withdrawal models
Regardless of the strong evidence suggesting a dominant
role for the right hemisphere on emotions, a number of early
studies reported a different pattern of brain asymmetry.
Goldstein (1939) showed that damage to the left hemisphere
was more likely to cause a catastrophic-depressive reaction
in psychiatric patients than damage to the right hemisphere.
Nelson Torro Alves and Sérgio Sheiji Fukusima, Departamento
de Psicologia e Educação, Faculdade de Filosoa, Ciências e
Letras de Ribeirão Preto, Universidade de São Paulo, Brazil. José
A. Aznar-Casanova, Departamento de Psicología Básica, Facultad
de Psicología, Universidad de Barcelona, Spain. Correspondence
concerning this article should be addressed to: Nelson Torro Alves,
FFCLRP - Universidade de São Paulo, Programa de Pós-Graduação
em Psicobiologia, Av. Bandeirantes, 3900. Monte Alegre. CEP:
14040-901, Ribeirão Preto – SP – Brasil. Phone: + 55-16-3602-4448,
Fax: + 55-16-3633-2660, E-mail: nelsontorro@yahoo.com.br
Psychology & Neuroscience, 2008, 1, 1, 63-66
DOI:10.3922/j.psns.2008.1.010
PSYCHOLOGY
NEUROSCIENCE
&
OPEN ACCESS
JOURNAL
Received 24 April 2007; received in revised form 26 February 2008; accepted 29 February 2008. Available online 20 May 2008
63_66_nelson_V02.indd 63 16/8/2008 14:51:52

64 Alves, Fukusima and Aznar-Casanova
Sackeim et al. (1982), reviewing 109 cases of pathological
laugh and crying, found evidence suggesting a differential
hemispheric specialization for positive and negative affect.
In general, damage to left hemisphere led to the onset of
depressive symptoms in psychiatric patients. On the other
hand, damage to the right hemisphere was more frequently
associated to a pathological laughing condition. Likewise,
Bear (1983) veried that lesions to the right hemisphere
tend to cause an indifference towards one’s own illness,
as well as nancial difculties, interpersonal conicts, and
other decits.
In order to deal with these results, a new brain
asymmetry model was proposed: the valence hypothesis
(Davidson, 1995). This model proposes that the pattern of
hemispheric dominance depends on the emotional valence
of the stimulus. The left hemisphere is dominant for
processing positive emotions whereas the right hemisphere
is dominant for processing negative emotions. According to
the valence hypothesis, fear, anger, disgust and sadness are
considered negative emotions, and happiness and surprise
are classied as positive emotions.
Recently, the motivational approach-withdrawal
hypothesis model has been proposed (Demaree, Everhart,
Youngstrom, & Harrison, 2005). This hypothesis
incorporates evolutionary concepts about the emotional
system, arguing that emotions are closely associated to the
behavior of the individual in its environment. According to
the approach-withdrawal hypothesis, happiness, surprise,
and anger are classied as approach emotions, since they
indicate a drive of the individual toward the environmental
stimuli. On the other hand, sadness, fear and disgust are
associated with withdrawal behaviors, because they tend
to lead the individual away from the environmental sources
of aversive stimulation. The negative/positive and the
approach/withdrawal models are very similar, but disagree
on the classication of the emotion of anger. In the negative/
positive model, anger is considered a negative emotion and
grouped together with sadness, fear, and disgust. However,
in the approach/withdrawal model, anger is considered
as an approach emotion, since it drives the individual to
the ght and the sources of stimulation, and is therefore
assigned to the same category as happiness and surprise. In
spite of this disagreement, both the valence and approach-
withdrawal hypotheses are similar and have received strong
support from many studies in the last decades (Demaree et
al., 2005).
Methods for studying brain asymmetry
Many methods have been used for assessing the
involvement of the cerebral hemispheres in the processing
of facial information. One of the earliest and most used
methods for studying brain asymmetry in normal subjects
is the divided visual eld technique. It was introduced
by Mishkin and Forgays (1952) and consists in the
tachistoscopic presentation of visual stimuli in the periphery
of the visual eld. Its adequacy for the study of hemispheric
processing is based on the anatomic properties of the visual
system. The visual system is arranged in such a way that
the temporal hemiretina sends the image to the ipsilateral
visual cortex, and the nasal hemiretina sends the image
to the contralateral visual cortex. Therefore, stimuli
presented in the left visual eld are initially projected
to the right hemisphere, whereas stimuli presented in
the right visual eld reach rst the left hemisphere. To
assure that the information will be processed initially by
only one hemisphere, two conditions are necessary: 1) the
stimulus must be presented to the left or to the right of
the xation point, in the periphery of the visual eld, 2)
the exposition time must be sufciently brief to prevent
that eye movements expose the visual stimulus to both
hemiretinas (Sergent, 1995). By analyzing reaction time
and judgment errors, it is possible to make inferences
about the functional asymmetry of the hemispheres.
Shorter reaction times and fewer judgment errors are
indicators that the hemisphere that rst processed the
stimulus is more involved in the processing of the
information investigated in the task.
This technique might be considered coarse when
compared to the current methods of study of the
cerebral functions. However, its simplicity and multiple
possibilities of manipulation of stimuli and tasks have
permitted researchers to make important inferences about
the functioning of the hemispheres. Reuter-Lorenz and
Davidson (1981) employed this technique to investigate the
hypothesis of the differential hemispheric specialization to
positive and negative emotions. The experiment consisted
in the presentation of an emotional and a neutral face on
the screen at the same time. One of the faces was presented
in the left visual eld and the other in the right visual eld.
They reported a relative superiority of the right hemisphere
for the perception of sad faces (shorter response times
for presentations in the left visual eld) and a relative
advantage of the left hemisphere for the perception of
happy faces (shorter response times for presentations in
the right visual eld).
Currently, modern neuroimaging techniques such
as fMRI, MEG, EEG, and PET, have revealed specic
areas related to the processing of facial stimuli. These
methods have also permitted scientists to establish
correlations between neurophysiologic activities and
emotional functions in the brain. A number of neuroimaging
studies have offered greater support to the approach-
withdrawal/positive-negative models by analyzing the
role of two important structures: the amygdala and the
prefrontal cortex.
The amygdala
The amygdala is a structure of the medial temporal l
obe implicated in a series of emotional processes (Le
Doux, 1995). Recent studies indicate that the amygdala plays
an important role in directing one’s attention to emotionally
salient stimuli and orienting the processing of stimuli
that have a major importance for the individual
(Davidson, 2003).
63_66_nelson_V02.indd 64 16/8/2008 14:51:52

Models of brain asymmetry in emotional processing 65
The amygdala has been associated with negative affect.
Lesions in this structure can reduce emotional responses
and impair the recognition of facial expressions of fear
and anger (Calder, Young, Rowland, Hodges, & Etcoff,
1996). Interestingly, worse performance in the perception
of voices of anger and fear has also been reported (Scott
et al., 1997).
Other studies have shown a positive correlation between
amygdala activation and severity of depression symptoms
in patients with major depressive disorder (Drevets et al.,
1992; Abercrombie et al., 1998). An enlargement of the
amygdala in depressed patients with bipolar disorders
(Altshuler, Bartzokis, Grieder, Curran, & Mintez, 1998)
and temporal lobe epilepsy (Tebartz, Woermann, Lemieux,
& Trimble, 1999) has also been found. In support to
the valence hypothesis, Mervaala et al. (2000) found a
reduction in the volume of the left amygdala in patients
with major depressive disorder.
The prefrontal cortex
The prefrontal cortex mediates the control of high-level
cognitive functions and is associated with the regulation of
many aspects of the affective system. It has been proposed
that the prefrontal cortex stores the representations of
goals and the means to achieve them, working in an
emotion-based decision making system (Davidson, 2003).
Patients with prefrontal cortex injury, especially in the
ventromedial area, are severely impaired in the decision-
making processes (Damasio, 1994).
Davidson (1995) showed that the prefrontal cortex is
a region of high affective asymmetry. The anterior region
of the left hemisphere is related to approach behaviors and
positive affects, whereas and the anterior portion of the
right hemisphere is associated with withdrawal behavior
and negative affects. Neuroimaging studies have offered
support to this idea. Jones and Fox (1992) found a greater
activation of the left hemisphere during the occurrence
of positive affect and a greater activation of the right
hemisphere in the presence of negative affect. The orbital
and ventral areas of the frontal cortex are implicated in
the representation of reward and punishment. O’ Doherty,
Kringelbach, Rolls, Hornak, and Andrew (2001) showed
that left orbitofrontal areas are especially responsive to
reward, whereas areas in the right orbitofrontal cortex are
more activated during punishment.
Perspectives for the study of brain
asymmetry
Some criticism has been directed towards the general
models of brain asymmetry. Many authors argue that the
level of specicity of the theories dealing with a whole
hemisphere is too coarse (Wager, Phan, Liberzon, & Taylor,
2003). An important issue refers to the absolute/relative
nature of the asymmetry. Early cognitive models tended
to conceive cognitive and emotional functions as located
exclusively in one hemisphere alone (Gainotti, 1972).
Scientists are now speaking about relative dominance, as
opposed to absolute dominance. Even strong lateralized
functions, such as language, are known to be distributed
in both hemispheres. The spoken language, for example,
requires structures of the left hemisphere for generating
grammatical sentences and syntax rules (e.g. Broca’s area),
whereas structures of the right hemisphere participate adding
the proper emotional intonation to speech (prosody). Both
linguistic components are important for the understanding
of speech. More recently, some studies have tried to
understand how the cerebral hemispheres cooperate and
coordinate their resources for processing information more
efciently (Tamietto et al., 2006).
Some authors have assumed that the investigation of
brain asymmetry must be focused on small regions of the
brain rather than on whole hemispheres. For example,
Wager et al. (2003) suggest that the whole hemisphere is too
general a unit of measure to be described by neuroimaging
data. Therefore, a more rened level of anatomic specicity
is necessary. These conclusions are based on a meta-
analysis of 65 neuroimaging studies, which investigated
brain asymmetry. They found no differences between the
cerebral hemispheres, when each one was analyzed as
a whole. However, when smaller brain structures were
compared, a more complex pattern of brain asymmetry
emerged from the data.
These results showed good evidence for the lateralization
of withdrawal/negative emotions in the left limbic system
(left insula, sublenticular extended amygdala and medial
frontal cortex). They also found limited support for left
lateralization of positive/approach emotions in the lateral
frontal cortex. Finally, they failed to show right-lateralized
activations for positive emotions.
Besides the debate on the absolute/relative nature of
brain asymmetry and the suggestion of a more rened level
of brain specicity, research must take into account other
fundamental characteristics of the emotional system. This
system can be conceived as a set of subsystems involved
in the processing of different aspects of the emotion.
Accordingly, Davidson (1995) proposed the division of the
emotional system in three distinct components leading with:
1) the perception of the emotion, 2) the experience of the
emotion and 3) the expression of the emotion. Moreover,
different neural substrates have been suggested for each
component. It is possible that some of the disagreement
between the valence and the right hemisphere hypotheses
might be explained by the fact that researchers are focusing
on different components of the emotional system. The
patterns of brain asymmetry for perceiving and expressing
emotions might not be the same.
Regardless of the number of studies supporting the right
hemisphere hypothesis; there is currently more evidence
favoring the valence/motivational model, especially for
the experience of the emotion (Davidson, 2003). Further
perspectives on this eld of study also indicate a fractioning
of the complex phenomenon of emotion into the analysis
of its basic components.
63_66_nelson_V02.indd 65 16/8/2008 14:51:52

66 Alves, Fukusima and Aznar-Casanova
Acknowledgment
This work was supported by grants from Brazilian
Nacional Research Council (CNPq) to Nelson T.
Alves (200321/2006-4) and to Sérgio S. Fukusima
(303592/2005-2).
References
Abercrombie, H.C, Schaefer, S.M, Larson, C.L., Oakes, T.R.,
Lindgren, K.A., Holden, J.E., Perlman, S.B., Turski, P.A., Kran,
D.D., Benca, R.M., & Davidson, R.J. (1998). Metabolic rate in
the right amygdala predicts negative affect in depressed patients.
Neuroreport, 9, 3301-3307.
Adolphs, R., Damasio, H., Tranel, D., & Damasio, A.R. (1996).
Cortical systems for the recognition of emotion in facial
expression. The Journal of Neuroscience, 16, 7678-7687.
Adolphs, R. (2002). Neural systems for recognizing emotion. Current
Opinion in Neurobiology, 12, 169-177.
Altshuler, L.L., Bartzokis, G., Grieder, T., Curran, J., & Mintez,
J. (1998). Amygdala enlargement in bipolar disorder and
hippocampal reduction in schizophrenia: An MRI study
demonstrating neuroanatomic specificity. Archives of General
Psychiatry, 55, 663-664.
Asthana, H.S., & Mandal, M.K. (2001). Visual-field bias in the
judgment of facial expression of emotion. Journal of General
Psychology, 128, 21-29.
Babinski, J. (1914). Contribution of cerebral hemispheric organization
in the study of mental troubles. Review Neurologique, 27,
845-848.
Bear, D.M. (1983). Hemispheric specialization and the neurology of
emotion. Neurological Review, 40, 195-202.
Blonder, L.X., Bowers, D., & Heilman, K.M. (1991). The role of the right
hemisphere in emotional communication. Brain, 114, 1115-1127.
Borod, J.C., Obler, K.L., Erhan, H.M., Grunwald, I.S., Cicero, B.A.,
Welkowitz, J., Santschi, C., Agosti, R.M., & Whalen, J.R. (1998).
Right hemisphere emotional perception: evidence across multiple
channels. Neuropsychology, 12, 446-458.
Bowers, D., Blonder, X.L., Feinberg, T., & Heilman, K.M. (1991).
Differential impact of right and left hemisphere lesions on facial
emotion and object imaginary. Brain, 114, 2593-2609.
Calder, A.J., Young, A.W., Rowland, D., Hodges, J.R., & Etcoff,
N.L. (1996). Facial emotion recognition after bilateral amygdala
damage: differentially severe impairment of fear. Cognitive
Neuropsychology, 13, 699-745.
Damasio, A. (1994). Descartes’ error. New York: Penguin Books.
Davidson, R.J. (1983). Hemispheric asymmetry and emotion. In R.J.
Davidson & P. Ekman (Eds.), Questions about emotions (pp. 39-
57). Massachusetts: MIT Press.
Davidson, R.J. (1995). Cerebral asymmetry, emotion, and affective
style. In R.J. Davidson & K. Hughdahl (Eds.), Brain Asymmetry
(pp. 361-387). Massachusetts: MIT Press.
Davidson, R.J. (2003). Affective neuroscience and psychophysiology:
toward a synthesis. Psychophysiology, 40, 655-665.
Demaree, H.A., Everhart, D.E., Youngstrom, E.A., & Harrison, D.W.
(2005). Brain lateralization of emotional processing: Historical
roots and a future incorporating “dominance”. Behavioral and
Cognitive Neuroscience Review, 4, 3-20.
Drevets, W.C., Videen, T.O., Price, J.L., Preskorn, S.H., Carmichael,
S.T., & Raichle, M.E. (1992). A functional anatomical study of
unipolar depression. Journal of Neuroscience, 12, 3628-3641.
Gainotti, G. (1972). Emotional behavior and hemispheric side of the
lesion. Cortex, 8, 41-55.
Goldstein, K. (1939). The Organism. New York: Academic Book.
Jansari, A., Tranel, D., & Adolphs, R. (2000). A valence-specific
lateral bias for discriminating emotional facial expressions in
free field. Cognition and Emotion, 14, 341-353.
Jones, N.A. & Fox, N. (1992). Electroencephalogram asymmetry
during emotionally evocative films and its relation to positive
and negative affectivity. Brain Cognition, 20, 280-299.
Ledoux, J.E. (1995). Emotion: clues from the brain. Annual Review
of Psychology, 46, 209-235.
Ley, R.G., & Bryden, M.P. (1979). Hemispheric difference in
processing emotions in faces. Brain and Language, 7, 127-138.
Mervaala, E., Fohr, J., Kononen, M., Valkonen-Korhonem, M.,
Vainio, P., Partamen, K., Artanen, J., Tiihonen, J., Viinamaki, K.,
Karjalainen, A.K., & Lehtonen, J. (2000). Quantitative MRI of the
hippocampus and amygdala in severe depression. Psychological
Medicine, 30, 117-125.
Mishkin, M., & Forgays, D.G. (1952). Word recognition as a function
of retinal locus. Journal of Experimental Psychology, 43, 43-48.
Mills, C.K. (1912). The cerebral mechanisms of emotional expression.
Transactions of the College of Physicians of Philadelphia, 34,
381-390.
O’ Doherty, J., Kringelbach, M.L., Rolls, E.T., Hornak, J., & Andrew,
C. (2001). Abstract reward and punishment representations in the
human orbitofrontal cortex. Nature Neuroscience, 4, 95-102.
Reuter-Lorenz, P., & Davidson, R.J. (1981). Differential contributions
of the cerebral hemispheres to the perception of happy and sad
faces. Neuropsychologia, 19, 609-613.
Rodway, P., Wright, L., & Hardie, S. (2003). The valence-specic
laterality effect in free viewing conditions: The inuence of sex,
handedness, and response bias. Brain and Cognition, 53, 452-463.
Sackeim, H.A., Gur, R.C., & Saucy, M.C. (1978). Emotions are
expressed more intensely on the left side of the face. Science,
202, 434-436.
Sackeim, H.A., Weiman, A. L., Gur, R.C., Greenberg, M. S.,
Hungerbuhler, J. P., & Geschwind, N. (1982). Pathological
laughing and crying: Functional brain asymmetry in the experience
of positive and negative emotions. Archives of Neurology, 39,
210-218.
Scott, K.S., Young, A.W., Calder, A.J., Hellawell, D.J.; Aggleton, J.P., &
Johnson, M. (1997). Impaired auditory recognition of fear and anger
following bilateral amygdala lesions. Nature, 385, 254-257.
Sergent, J. (1995). Hemispheric contribution to face processing:
patterns of convergence and divergence. In R. J. Davidson & K.
Hughdahl (Eds.), Brain Asymmetry (pp.157-181). Massachusetts:
MIT Press.
Tamietto, M., Corazzini, L.L., Gelder, B., & Geminiani, G. (2006).
Functional asymmetry and interhemispheric cooperation in the
perception of emotions from facial expressions. Experimental
Brain Research, 171, 389-404.
Tebartz, V.E., Woermann, F.G., Lemieux, L., & Trimble, M.R.
(1999). Amygdala enlargement in dysthymia - A volumetric study
of patients with temporal lobe epilepsy. Biological Psychiatry,
46, 1614-1623.
Wager, T.D., Luan Phan, K., Liberzon, I., & Taylor, S.F. (2003).
Valence, gender, and lateralization of functional brain anatomy
in emotion: a meta-analysis of findings from neuroimaging.
Neuroimage, 19, 513-531.
po
63_66_nelson_V02.indd 66 16/8/2008 14:51:53