Emotions and the Right Hemisphere: Can New Data Clarify Old Models?

Abstract

Models advanced to explain hemispheric asymmetries in representation of emotions will be discussed following their historical progression. First, the clinical observations that have suggested a general dominance of the right hemisphere for all kinds of emotions will be reviewed. Then the experimental investigations that have led to proposal of a different hemispheric specialization for positive versus negative emotions (valence hypothesis) or, alternatively, for approach versus avoidance tendencies (motivational hypothesis) will be surveyed. The discussion of these general models will be followed by a review of recent studies which have documented laterality effects within specific brain structures, known to play a critical role in different components of emotions, namely the amygdata in the computation of emotionally laden stimuli, the ventromedial prefrontal cortex in the integration between cognition and emotion and in the control of impulsive reactions and the anterior insula in the conscious experience of emotion. Results of these recent investigations support and provide an updated integrated version of early models assuming a general right hemisphere dominance for all kinds of emotions.

Keywords

laterality of emotions right hemisphere hypothesis valence hypothesis unconscious emotions and the right amygdala right ventromedial prefrontal cortex and emotional control right anterior insular cortex and emotional experience

The First Descriptions and Interpretations of a Different Emotional Behavior in Patients with Right and Left Hemispheric Lesions

The hypothesis assuming that hemispheric asymmetries may exist in the representation of emotions is recent and controversial. It is recent, because a century elapsed between the first studies showing a left hemisphere (LH) dominance for language (Broca 1865; Dax 1865) and the first investigations showing laterality effects in the representation of emotions (Gainotti 1969, 1972; Rossi and Rosadini 1967; Terzian and Cecotto 1959). It was, and remains, controversial because different models of emotional lateralization were advanced, since these pioneering investigations, to clarify the meaning of the observed asymmetries. Terzian and Cecotto (1959) and Rossi and Rosadini (1967), who first described a different emotional behavior in patients submitted to pharmacological inactivation of the right and LH, relied on the model of the bipolar manic depressive disorders to explain their observations. They reported that injection of sodium amytal into the left carotid artery produces a “depressive-catastrophic reaction” (characterized by a sad attitude with bursts of tears), whereas inactivation of the right hemisphere (RH) is followed by a “euphoric-maniacal reaction” and attributed these different emotional reactions to disruption of neural mechanisms underpinning opposite aspects of mood. Depressive-catastrophic reactions were attributed to inactivation of a center for positive emotions located in the LH and euphoric-maniacal reactions to disruption of a center for negative emotions located in the RH. On the other hand, Gainotti (1969, 1972), who some years later made partly similar observations in right and left brain-damaged patients, describing “catastrophic reactions” in (aphasic) left, and “indifference reactions” in severe right brain–damaged patients, refuted the equivalence between catastrophic reactions and biological depression and between indifference reactions and euphoric-maniacal states. He considered catastrophic reactions as a dramatic, but psychologically appropriate form of response to a catastrophical event, and the indifference reaction of patients with severe RH lesions as an abnormal or inappropriate reaction to a dramatic event. To explain the contrast between the different emotional behavior of right brain– and left brain–damaged patients, Gainotti (1972) advanced the hypothesis that the RH may be dominant for emotion, just as the LH is dominant for language and that the emotional reaction may be inappropriate in right brain–damaged patients if the lesion disrupted structures crucially involved in emotional processing. Thus, the first clinical observations that have raised the problem of hemispheric asymmetries in emotion representation have also prompted the two models of emotional lateralization that are still considered as the most important ones in this area of inquiry and which can be labeled as “the right hemisphere” hypothesis and “the different hemispheric specialization” (or “the valence”) hypothesis. The first model supposes a general dominance of the RH for every kind of emotional response, regardless of affective valence, whereas the second model assumes an opposite dominance of the LH for positive and of the RH for negative emotions.

Models of Human Emotions that Have Oriented Investigations of Emotional Laterality in the Human Brain

The general model of emotions to which most subsequent investigations of emotional laterality in the human brain made reference was the Ekman’s (1977, 1984) model. This model, drawing on the Darwin’s (1872) claim that facial expression of emotions is part of man’s biological inheritance, maintained that the human expressive mimic reactions are automatically selected from a small number of innate operative patterns, corresponding to the basic emotions (happiness and sadness, fear and anger, surprise and disgust). This theoretical framework was greatly expanded by other authors (e.g., Frijda 1986; Izard 1977; LeDoux 1996; Panksepp 1989; Plutchik 1980) who considered emotion as a multicomponent adaptive system, whose functional architecture has developed across phylogeny, spanning from very primitive, hard-wired survival-related behavioral schemata to much more complex and learned social patterns, integrated with the cognitive system.

Relationships Between the Emotional and the Cognitive System

Oatley and Johnson-Laird (1987) maintained that the organism disposes of two operative systems to face a partially unpredictable environment: (1) the emotional system, considered as an emergency system, able to interrupt the ongoing activity to rapidly select a new operative scheme and (2) the cognitive system, viewed as a more complex and evolved system, but requiring much more time to accomplish its work. Both structural similarities and functional differences exist between emotional and cognitive system. The structural similarities stem from the fact that both systems base their activity on the integrated work of components that must (1) analyze the sensory data to compute their significance, (2) select the most suitable responses, and (3) put all this information into appropriate memory systems. The functional differences (which derive from the logic of the two systems and concern the manner in which each system deals with sensory information and selects specific action schemata) are reported in Box 1.

Box 1.

Common aspects and distinguishing features of the emotional and cognitive systems.

Emotional and Cognitive Systems
Common Aspects. Both are phylogenetically advanced adaptive systems based on the integrated activity of components that must process ongoing information, select the most appropriate behavioral response and keep a memory of the whole event
Distinguishing Features
Cognitive System	Emotional System
Information Processing
Exhaustive but slower computation of highly processed data leading often to gather further information	Quick computation of crude, poorly processed relevant sensory data, leading to a positive or negative evaluation of stimulus significance and to a direct motor response. The amygdala plays a critical role from this point of view, through both a fast subcortical and the slower classical cortical route
Behavioral response
The selection of the operative strategy results from a thorough analysis of the external situation and of memory stored data. It can consist of an immediate or delayed action or of the inhibition of an inappropriate motor response	Automatically selected from a small number of innate schemata corresponding to the survival needs of the species. These basic neuro-motor programs include facial and vocal expressive components, allowing emotional communication and postural components, conveying appropriate action tendencies. The ventro-medial prefrontal cortex (vmPFC) is involved in the integration between cognition and emotion and in the control of impulsive reactions
Level of vegetative activation
A low activation of the autonomic nervous system is usually observed during cognitive tasks	A high level of activation of the autonomic nervous system is integral part of the emotional experience, with a prevalent activity of the sympathetic system during challenging negative emotions. The insular cortex strongly contributes to the conscious experience of emotion, integrating lower level homeostatic representations with higher level cognitive functions
Learning mechanisms
Based on the controlled and conscious declarative memory system	Based on conditioned, automatic and unconscious learning. The amygdala plays a critical role in classical conditioning of emotional stimuli

In addition to describing the typical features of the emotional system in these different functions, in Box 1 are also reported the brain structures that play a critical role in each of them, namely, the amygdala in the quick and raw computation of sensory data, the ventro-medial prefrontal cortex (vmPFC) in the integration between cognition and emotion and the control of inappropriate emotional reactions, and the insular cortex in providing a substrate to the conscious experience of emotion. In later sections of the present review, laterality effects within each of these brain structures will be taken separately into account, to evaluate their contribution to hemispheric asymmetries in emotion processing and representation.

Hierarchical Organization of the Emotional System

The acknowledgment that emotional and cognitive systems become more and more interconnected during the development prompted the construction of hierarchically organized developmental models of emotions, that aimed to explain how complex emotions can be formed starting from the simplest ones and how the highest components keep under control the lowest parts of the emotional system. In particular, Leventhal (1974, 1987) proposed a developmental model which assumed that human emotions may be based on three functional levels: (1) the sensorimotor, (2) the schematic, and (3) the conceptual level. The sensorimotor level consists of a set of innate, universal expressive-motor programs, which are triggered automatically by a certain number of stimuli and include components of motor and autonomic activation, as well as the corresponding subjective emotional feelings. The schematic level results by the association, during the individual development, of these innate programs with situations of individual experience. This leads to the construction of “emotional schemata,” which are automatically elicited, correspond to spontaneous emotions and are accompanied by subjective feelings, which are the hallmarks of a true emotion. The conceptual level, which is the last stage of this model, is based on mechanisms of conscious declarative memory and does not store instances of concrete emotional experiences, but abstract notions about emotions and about the social rules allowing their expression.

Early Experimental Investigations that Have Evaluated Comprehension or Expression of Positive and Negative Emotions at the Facial or Vocal Level

In the years following the first descriptions of a different emotional behavior in patients with right and left hemispheric lesions, several experimental investigations were conducted in healthy subjects and in patients with unilateral brain injury, to clarify the meaning of the different emotional reactions observed in unilateral brain-damaged patients. Since the easiest manner of studying positive and negative emotions consists in contrasting their expression at the facial or vocal level, these investigations used methodologies that evaluated comprehension or production of positive and negative emotions through facial expression or vocal emotional prosody. In investigations conducted on normal subjects, the monohemispheric treatment of emotional information was studied both in the visual modality (lateralized tachistoscopic presentation) and in the auditory modality (dichotic listening or lateralized auditory presentation), whereas hemispheric asymmetries on the expressive side were studied primarily by comparing the emotional expressiveness of the two hemifaces. Box 2 reports some data about methodology and results obtained in these studies.

Box 2.

Methodology and results of investigations that have studied comprehension and expression of emotions in normal subjects through the affective tone of voice or facial emotional expressions.

Comprehension of auditory emotional stimuli.
Using the dichotic listening technique, Haggard and Parkinson (1971), Carmon and Nachshon (1973), Ley and Bryden (1982), and Bryden (1982) showed an overall left ear (right hemisphere) advantage in the recognition of nonverbal emotional sounds and emotional prosody. Results consistent with the right hemisphere advantage in emotional prosody processing were more recently obtained by Voyer and others (2002) assessing the reliability of laterality effects in dichotic emotion recognition tasks and by Vingerhoets and others (2003) studying cerebral hemodynamics during discrimination of prosodic and semantic emotion in speech.
Recognition of facial emotional expressions.
Using a tachistoscopic lateralized presentation of emotional faces to the right and left visual field, Suberi and McKeever (1977), Buchtel and others (1978), Landis and others (1979), Ladavas and others (1980), Strauss and Moscovitch (1981), Heller and Levy (1981), Duda and Brown (1984), Kinsbourne and Bemporad (1984), Mandal and Singh (1990), Hugdahl and others (1993) and Asthana and Mandal (2001) showed an overall left visual field (right hemisphere) advantage. In line with these results were data obtained by Killgore and Yurgelun-Todd (2007) studying healthy participants who viewed two split visual-field facial emotional pictures during functional magnetic resonance imaging. Results suggested that the posterior right hemisphere is activated during non-conscious emotional face perception regardless of affective valence, even if greater activation is produced by negative facial cues. Ahern and Schwartz (1979), Reuter-Lorenz and Davidson (1981), Reuter-Lorenz and others (1983), and Natale and others (1983) documented, however, a greater right hemisphere involvement in perception of negative emotions and a greater left hemisphere involvement in perception of positive emotions and partly similar results were obtained by Rodway and others (2003).
Responsiveness to emotional stimuli.
Wittling and Roschmann (1993) presenting positive and negative films, documented a higher subjective emotional response to both kinds of emotional stimuli when they were shown to the right hemisphere.
Spontaneous and posed facial expressions of emotions.
Using video records of spontaneous emotions, Moscovitch and Olds (1982), Dopson and others (1984), and Wylie and Goodale (1988) could demonstrate a general right hemisphere dominance in facial expression of felt emotions. Similar results were obtained studying posed, rather than spontaneous expressions of emotions. In most of these studies subjects were photographed while posing positive or negative emotions, then composite photographs were created, using two left or two right half faces, and rated for intensity. Borod and others (1988), Moreno and others (1990), Asthana and Mandal (1998), and Nicholls and others (2002) found that both positive and negative left-left composites were judged as having expressed emotions more intensely than the right-right composites. However, Sackeim and Gur (1978), Heller and Levy (1981), Sackeim and Grega (1987), Schiff and Lamon (1989), and Mandal and Singh (1990) found a left-sided facial asymmetry for negative but not for positive emotions.

Data reported in Box 2 show that comprehension and expression of emotions through face and voice are lateralized to a great extent in the RH, regardless of valence. Consistent with data obtained in normal subjects were results of investigations which studied comprehension and expression of positive and negative emotions in patients with unilateral brain lesions, comparing the ability of right brain– and left brain–damaged patients to recognize or express emotions both with voice (emotional prosody) and with facial expression. Some authors did, indeed, show that right brain–damaged patients can understand the meaning of a sentence, but are unable to recognise the emotion expressed by the tone of voice of the speaker (see Ross 1981, 1984; Gainotti 2000, 2001; and Ross and Monnot 2007 for reviews). Other authors showed that patients with RH damage are seriously impaired in recognizing facial emotional expressions (see Mandal and others 1993; Gainotti 2001, 2005; and Borod and others 2002 for reviewes). Similar results were obtained studying the capacity of right brain– and left brain–damaged patients to express emotions through the tone of voice (see Ross 1981, 1984; Gainotti 2000, 2001; Ross and Monnot 2007 for reviews) and through facial emotional expression (see Borod and others 1986; Mandal and Ambady 2004; and Gainotti, 2001, 2005 for reviews). Altough most data obtained in normal subjects and in unilateral brain-damaged patients strongly support the hypothesis of a general RH dominance for emotional comprehension and expression, results of some investigations conducted in normal subjects with different experimental procedures (and also reported in Box 2) could support the hypothesis of a different specialization of the RH for negative emotions and of the LH for positive emotions. Thus, Reuter-Lorenz and Davidson (1981), Reuter-Lorenz and others (1983), Natale and others (1983), and Rodway and others (2003) documented a RH involvement in comprehension of negative emotion and a LH involvement in comprehension of positive emotions, whereas Sackeim and Gur (1978), Heller and Levy (1981), Sackeim and Grega (1987), Schiff and Lamon (1989), and Mandal and Singh (1990) found a greater left-sided intensity in facial expression of emotions only for negative, but not for positive emotions.

Models of Emotional Laterality Prompted by the Aforementioned Studies of Comprehension and Expression of Positive and Negative Emotions

Three main models of emotional laterality came from the aforementioned studies of comprehension and expression of positive and negative emotions at the facial or vocal level. The first model stressed the RH superiority in comprehension and expression of emotions, assuming that the RH dominance for emotions may basically concern their communicative aspects. The second model emphasized the greater hemiface asymmetry for negative with regard to positive emotions. The third model assumed that hemispheric asymmetries observed at the level of the frontal lobes during positive and negative emotions, may not be related to the valence of the emotional stimuli but rather to the motivational (approach vs. avoidance) systems engaged by these stimuli. Each of these models will be separately taken into account in the present review.

The Model Assuming that the Right Hemisphere Dominance for Emotions May Only Concern the Communicative Aspects of Emotions

This model was proposed by Ross (1981, 1984), who maintained that disorders of emotional communication are the primary defect resulting from RH damage and that other emotional disturbances of right brain–damaged patients are only a consequence of this basic inability to comprehend and express emotions. This viewpoint was, however, at variance with results obtained by Wittling (1990) in healthy subjects and by Heilman and others (1978), Morrow and others (1981), and Zoccolotti and others (1982, 1986) in brain-damaged patients. Wittling (1990) studied blood pressure changes during lateralized presentation of an emotional film and showed that RH film presentation caused a significantly higher increase in systolic and diastolic pressure than LH viewing of the same film. In a similar vein, Heilman and others (1978), Morrow and others (1981), and Zoccolotti and others (1982, 1986) showed that right brain–damaged patients present not only disorders of emotional communication but also a flattened galvanic skin response (GSR) to painful or distressing emotional stimuli. Taken together, these data show that right brain damage disrupts not only the communicative aspects but also the autonomic components of emotions.

The Greater Hemiface Asymmetry for Negative Emotions and the Social Use of Smile and Other Positive Facial Expressions

Etcoff (1986) noted that smiling differs from other emotional facial expressions not only because of its positive emotional polarity, but also because it represents the most easy “emotional” facial expression to reproduce voluntarily and the most currently used for approach and social communication. She, therefore, claimed that, in the case of smiling, a LH dominance for the intentional control of the facial expressive apparatus could counterbalance the greater left half-face expressiveness, resulting from the general RH prevalence for the spontaneous expression of emotions. A partly similar interpretation was advanced by Gainotti and others (1993), drawing on the distinction proposed by Leventhal (1974, 1987) between “schematic” and “conceptual” levels of emotions. These authors suggested that the RH might be involved preferentially in the spontaneous expression of emotions, whereas the left frontal lobe might be mainly involved in the intentional control of the emotional expressive apparatus. Results consistent with this line of thought were recently obtained by Ross and Pulusu (2013) contrasting spontaneous with posed facial emotional expressions, because these authors showed that spontaneous (schematic) expressions are usually initiated on the left side of the face, whereas posed expressions (linked to social communication and associated display rules) are initiated on the right side of the face.

The Davidson Hypothesis Assuming that Frontal Lobe Asymmetries May Not Be Related to Emotional Valence but to the Motivational Systems Engaged by the Stimuli

Drawing on electroencephalography (EEG) asymmetries observed by Davidson and others (1979) and by Davidson and Fox (1982) at the level of the frontal lobes during positive and negative emotions, Davidson (1983, 1992, 1998) claimed that these asymmetries were not related to the valence of the emotional stimuli but to the motivational systems engaged by these stimuli. This author proposed that the left prefrontal cortex (PFC) may be involved in a system facilitating approach to appetitive stimuli, whereas the right PFC may be involved in a system facilitating withdrawal from aversive stimuli. According to Davidson (1992), the arousal of approach-related emotions should be associated with activation of the left, and arousal of withdrawal-related emotions with activation of the right frontal region. Even if after the 1990 the measure of the frontal EEG asymmetries and the motivational approach-avoidance model became extremely popular, pruducing hundreds of research articles, both the relation between PFC and approach/avoidance and the use of frontal EEG asymmetries to assess emotion or motivation have been the object of documented critical reviews (e.g., Spielberg and others 2008 for the first issue and Allen and others 2018 and Reznik and Allen, 2018 for the second methodological problem). Furthermore, some authors have challenged the equivalence approach—positive and avoidance—negative emotions, stressing the fact that anger, which is a negative emotion (Russell and Barrett 1999), often evokes an approach motivation and usually coincides with activation of the left hemisphere (Carver and Harmon-Jones 2009). More in general, it must be acknowledged that, even if this model has been very influential, it can hardly explain results of the experimental and clinical studies reported in Box 2 of the present review for at least two reasons. The first is that the difference between positive and negative emotions studied at the expressive level in the aforementioned investigations is only in part captured by the distintion between approach and withdrawal tendencies proposed by Davidson (1983, 1992, 1998). The second reason is that the aforementioned studies have shown that the RH dominance concerns not only the expression of emotions, subserved by the anterior frontal regions, but also the recognition of emotionally laden information, subserved by posterior cerebral cortices. Instead, the approach/ withdrawal model only concerns the experience and expression of emotions at the level of the PFC. A general dominance of the RH in the processing of emotional information has, indeed, been acknowledged by Davidson (1983), who suggested an interaction between the right/left and the anterior/posterior dichotomy in the regulation of human emotions. This interactive account assumed an overall dominance of the right parietal region for the treatment of emotional information and a diverging specialization of the right and left frontal lobes for the expression of negative and positive emotions. However, if this model was correct, we should predict that the interaction between valence and laterality should be greater at the expressive than at the receptive level, whereas data reported in Box 2 show a mild trend in the opposite direction, istead of supporting this prediction.

Perplexities about Existence and Nature of a Lateralization of Emotional Functions Drawn from Functional Neuroimaging Studies of the Neural Correlates of Emotions

Data relevant to the existence and nature of a lateralization of emotional functions can be drawn from the study, using positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), of the activation produced in various brain structures of healthy subjects by experimental paradigms assessing different facets of emotions. Several authors, therefore, explored the neuroanatomical substrates of emotions using different emotional categories, experimental paradigms and kinds of stimuli. To give an overall survey of these studies, Wager and others (2003) performed a quantitative meta-analysis on 65 neuroimaging studies of emotion focusing on the effects of emotional valence on regional brain activations, with particular emphasis on hypotheses concerning lateralization of brain function in emotion. These authors found no support for the hypothesis of overall right-lateralization of emotional function, and limited support for valence-specific lateralization of emotional activity in frontal cortex. Similar results were obtained by Fusar-Poli and others (2009) in a voxel-based meta-analysis of studies employing emotional faces paradigms in healthy subjects, because this study too failed to support both the “right hemisphere” and the “valence” hypothesis. These rather disappointing results must be considered with caution, because they can be due to several factors concerning both methodological and experimental reasons. For instance, constraints and limits imposed by functional imaging methodologies constitute a far from ideal environment for studying full-blown emotional processes. Thus, Levenson and others (2014) noticed that, even if it were possible to induce powerful emotions in the scanner, the attendant muscular activity in body and face would produce huge signal artifacts. As a result, a great deal of emotional research conducted in the scanner falls into the domain of emotional cognition (where the focus is on how we think about emotions and make judgments about them), rather than the actual processes as they unfold in real time. More interesting than results obtained on heterogeneous whole brain activation studies must, therefore, be considered data obtained in anatomo-clinical or activation studies of brain structures, such as the amygdala, the vmPFC and the anterior insula, that, as shown previously and in Box 1 of this review, play very relevant roles in specific components of emotional functions. A diagram showing the functional interactions between these components of the emotional system is reported in Figure 1.

Figure 1.

Schematic representation of the functional interactions existing between the main components of the emotional system. Bilateral connections exist between the amygdala (where emotional information is computed), the orbitofrontal cortex (where they are integrated with social rules allowing emotional expression), and the anterior insular cortex (which contributes to the conscious experience of emotions). The uncinate fasciculus connects the anterior portions of the temporal lobe (temporal pole and amygdala) with the inferior frontal gyrus, passing inward of the insular cortex and allowing a “topdown” modulation of intense emotional responses.

Investigations that Have Documented a Different Role of Right and Left Amygdala in the Evaluation of Emotional Stimuli

A very influential role, within the anatomo-clinical and activation studies that have proposed a different role of the right and left amygdala in emotional functions, was played by Morris and others (1998), who showed that stimuli processed below the level of awareness mainly activate the right amygdala, whereas consciously processed emotional stimuli preferentially activate the left amygdala. Trying to elucidate the neural mechanism that could subsume this dissociation, Morris and others (1999) documented a different functional connectivity of right and left colliculo-pulvinar pathways during processing of seen and unseen (masked) fear-conditioned faces. Increased connectivity between right amygdala, pulvinar, and superior colliculus was found when masked fear-conditioned faces were presented, whereas the left amygdala showed no masking-dependent changes in connectivity with superior colliculus or pulvinar. In line with this model, Wright and others (2003) and Gläscher and Adolphs (2003) proposed that the right amygdala might be involved in the rapid detection of emotional stimuli, while the left amygdala could play a role in the more elaborate stimulus evaluation. A selective right amygdala activation during unconscious processing of emotional stimuli was also reported by Nomura and others (2004) during cognitive evaluation of facial expressions primed by masked angry faces, because activity in the right amygdala was greater with subliminal presentation of the angry prime compared with subliminal presentation of a neutral face or white-blank stimuli. Williams and others (2006) also used fMRI in healthy human subjects to study the functional connectivity between amygdala and related cortical and subcortical structures during conscious and non-conscious perception of fearful facial expressions. Conscious perception was associated with negative connectivity but non-conscious perception with positive connectivity between superior colliculus, pulvinar and right amygdala. Hung and others (2010), studying with magnetoencephalography (MEG), the effect on event-related neural responses of unattended emotional faces, located in the left or right visual fields confirmed that that the amygdala processes threat-related information through a right fast subcortical route and a left slower cortical feedback mechanism (see Gainotti 2012a for a more detailed description of the aforementioned investigations).

Activation and Lesion Studies Documenting Asymmetries of Emotional Functions in the Ventro-medial Prefrontal Cortex

The right vmPFC may have a “general” role in emotional processing (see Drevets and Raichle 1998 for review), in the integration between cognition and emotion and in the control of impulsive reactions. As for the first point, Shamay-Tsoory and others (2003) claimed that the right vmPFC regulates the interaction of emotion and cognition in the production of empathic responses and the same authors (Shamay-Tsoory and others 2005) maintained that impaired “affective” theory of mind (TOM) is associated with right vmPFC damage. As for the second issue, Tranel and others (2002) demonstrated that patients with lesions of the right vmPFC show considerably more deficits in social, emotional, and decision-making domains than those with left-sided lesions. In a similar vein, Zald and Andreotti (2010) showed that damage to the vmPFC (especially in the right hemisphere) is connected with deficits in detecting irony, sarcasm, and deception, whereas Boes and others (2009) found a significant correlation between low impulse control and decreased right vmPFC volume in impulsive boys. These data are consistent with the the positions of Aron and others (2004 and 2014), who reviewed evidence suggesting that a sector of the right inferior frontal cortex (rIFC) implements a general inhibitory control via a wider prefrontal-basal ganglia network. All these data suggest a right lateralization of functions subsumed by the the ventral PFC, because this structure plays a critical role in the integration between cognition and emotion and in functions of “topdown” modulation of intense emotional responses, thanks to its connections with the amygdala through the uncinated fasciculus (UF), as is shown in Figure 1. Consistent with these views are data showing that connections between anterior temporal lobe (ATL) and orbito-frontal areas (through the UF) are stronger in the RH, while connections between ATL and inferior frontal gyrus (through the arcuate fasciculus), which have a key role in phonological processing are greater in the LH (Papinutto and others 2016). The relationships between right UF and and emotional functions were also documented by Coad and others (2017), who showed that in healthy subjects’ interindividual variability in the ability to decode facial emotion expressions is linked to the right hemisphere UF microstructure.

The Contribution of Right and Left Insular Cortex to Conscious Experience of Emotion

Since the insula is known to contain the primary gustatory cortex, earlier studies had focused on its special role in disgust (an emotion closely associated with the sensation of bad taste). In recent years, however, more emphasis has been placed on the insular contribution to conscious experience of emotion, because this experience depends on the perception of bodily reactions to emotion-provoking objects and the cognitive interpretation of these interoceptive informations. The insula receives interoceptive inputs from the whole body, and has bidirectional connections with the frontal, parietal, and temporal lobes, the anterior cingulate cortex and the amygdala. This connectivity pattern allows to integrate lower level homeostatic representations with higher level cognitive functions. Craig (2009, 2010, 2011) therefore proposed a posterior-to-anterior gradient in the insular cortex, in which physical features of interoception are processed in the posterior insula and the integration of interoception with cognitive and motivational information is made in the anterior insular cortex (AIC). A schematic representation of the integration of homeostatic and cognitive aspects of the conscious experience of emotions in the right AIC is reported in Figure 2.

Figure 2.

The figure shows in a schematic manner how interoceptive inputs coming from the whole body, through the spino-thalamic tracts, the ventral posterior thalamic nuclei and the secondary somatosensory cortices, reach the posterior insula providing first-order homeostatic representations. The figure also shows how the anterior insular cortex (and in particular the right anterior insula) thanks to its connections with the amygdala, the frontal cortices, and the anterior cingulate cortex, integrates lower level homeostatic representations with higher level cognitive functions and becomes the substrate of the conscious experience of emotions.

Craig (2005) also proposed a major contribution of the right AIC to the emotional experience and assumed that this hemispheric asymmetry may be based on an unequal representation of homeostatic activities, resulting from asymmetries in the peripheral autonomic nervous system. Results consistent with a greater role of the right insula in homeostatic representations were obtained by Critchley and others (2004), who measured regional brain activity by fMRI during an interoceptive task wherein subjects judged the timing of their own heartbeats. These authors observed that neural activity in right AIC predicted subjects’ accuracy in the heartbeat detection task and that greater AIC volume correlated with increased accuracy in this subjective sense of the inner body, and with the corresponding negative emotional experience. Their interpretation of these results was that the right AIC supports a representation of visceral responses accessible to awareness and provides a substrate for subjective feeling states. Results consistent with these views were obtained by by Gray and others (2007), who scanned participants while judging emotional face stimuli, during both exercise and non-exercise conditions in the context of true and false auditory feedback of tonic heart rate and by Xue and others (2010), who showed that the experience of taking (and especially winning) a gamble was associated with significantly stronger activation in the right AIC. From the neuroanatomical point of view, the greater role of the right AIC in emotional functions, cound be due to prevalence on this side of the von Economo neurons (VENs), which project from the frontoinsular (FI) cortex to frontal pole, septum, and amygdala, relaying to these structures information related to autonomic control or awareness of homeostatic representations. According to Allman and others (2010), these neurons are about 30% more numerous in the right than in the left FI cortex.

General Discussion

The aim of this discussion will consist in trying to summarize results obtained in various sections of this review with respect to the general problem of models advanced to explain the lateralization of emotional functions in the human brain and to see if results obtained in more recent studies can clarify those of more ancient investigations. The first clinical observations made on patients with focal brain damage by Gainotti (1972) and the first clinical and experimental studies which have investigated comprehension and expression of emotions at the facial or vocal level have generally suggested a greater involvement of the RH in emotional functions, irrespectively of their positive or negative valence (see Borod and others 1997, 2001; Gainotti 2001, 2005; and Mandal and Ambady 2004 for critical reviews). The hypothesis of a different lateralization of positive and negative emotions was supported only by a small number of experimental studies conducted in healthy subjects but became very influential when it was reframed in terms of approach versus withdrawal motivational tendencies. This hypothesis was advanced by Davidson (1983, 1992, 1998) relying on EEG asymmetries observed at the level of the frontal lobes during positive and negative emotions, but in recent years Allen and others (2018) and Reznik and Allen (2018) have raised strong methodological objections to the use of frontal EEG asymmetries to assess emotion or motivation. Furthermore, a careful inspection of data repported in in Box 2 shows that investigations which had studied in healthy subjects the expression of positive and negative emotions had not documented a greater involvement of the RH and LH in the production of negative and, respectively, of positive emotions, but only a greater engagement of the RH in the generation of negative, in comparison with positive, emotions. The observation of a greater expressivity of the left hemiface for negative emotions than for smiling or other positive emotions had, therefore, been interpreted by Gainotti and others (1993) and by Ross and Pulusu (2013) as related more to a greater involvement of the RH in the spontaneous expression of emotions and of the left frontal lobe in functions of emotional control than to the distinction between negative and positive emotions. Recent studies that have documented asymmetries of emotional functions in the ventro-medial PFC (Aron and others 2004, 2014; Boes and others 2009; Tranel and others 2002) are, however, at variance with this model, because they suggest a right lateralization of all emotional functions subsumed by these structures, including the “topdown” modulation of impulsive emotional reactions.

Other investigations that have tried to clarify the mechanisms underlying the processing of emotional information at the level of the right and left amygdala and the experience of emotions in the anterior insular cortex are also consistent with the model assuming a general dominance of the RH for various aspects of emotional functioning. Several functional neuroimaging experiments have, indeed, been pioneered by the influential articles of Morris and others (1998 and 1999) on conscious and unconscious forms of emotional learning in the human amygdala and by results of fMRI experiments conducted by Critchley and others (2004) and Gray and others (2007) to evaluate the contribution of the anterior insula to the conscious experience of emotions. These experiments have consistently shown: (1) that stimuli processed below the level of awareness mainly activate the right amygdala, whereas consciously processed emotional stimuli preferentially activate the left amygdala; (2) that the right amygdala activation during unconscious treatment of emotional stimuli is due to an increased connectivity between right amygdala, pulvinar, and superior colliculus whereas an involvement of this subcortical pathway is not observed when emotional stimuli are consciously processed; and (3) that the right AIC supports a representation of visceral responses accessible to awareness and provides a substrate for subjective emotional feelings. A model that according to Gainotti (2005, 2007a, 2007b) could explain the relationships between unconscious emotional processing and right amygdala activation through a subcortical visual pathway draws on the general account that many authors (e.g., Ekman 1984; Frijda 1986; LeDoux 1996; Panksepp 1989) have given of emotion, considered as a phylogenetically older, automatic and poorly controlled emergency adaptive system. The Gainotti’s (2005 and 2007a) model assumes that the non-verbal functional organization of the RH may be considered as more primitive than the verbal functional organization of the LH and may be caracterized by a higher degree of reliance on sensorimotor functions, emotional processing, unawareness, and automaticity, whereas the LH’s functional organization might be characterized by a prevalence of verbal cognitive processing, consciousness and intentionality. This model could explain the different format of conceptual and familiar people representations, which are stored in a sensory non-verbal format in the right anterior temporal lobe ATL and in a verbal modality in the left ATL (Gainotti 2007b, 2012b, 2015). It could also explain some automatic functions typical of the RH, such as the automatic generation of familiarity feelings, involved in the recognition of facial identity (Gainotti 2007a) and the disruption of the automatic components of the spatial orienting of attention that charaterizes the RH syndrome of unilateral spatial neglect (see Gainotti 1996 for a critical review). As for the properly emotional functions, this model could explain both the persistence in the RH of a more primitive treatment of emotions through the subcortical pathway (LeDoux 1996; Tamietto and de Gelder 2010) and the greater involvement of the RH in comprehension and expression of negative emotions, because the definition of emotions as a phylogenetically old emergency system could apply more to danger-related negative emotions than to positive and social types of emotions. Consistent with the aforementioned model are also results of activation studies, conducted by Critchley and others (2004) and Gray and others (2007), which have shown that even the subjective emotional feelings, that are the distinctive feature of spontaneous emotions, are mainly subsumed by RH structures, and, in particular by the right AIC, which represents emotional experience, because it receives and integrates interoceptive inputs from the whole body, guiding second-order “cognitive” representations of bodily arousal state. Taken together, all these investigations, which have shown that the right amydgala plays a critical role in the early assessment of emotional stimuli, the right anterior insula provides the substrate for subjective feeling states and the right vmPFC is involved in the control and “topdown” modulation of intense emotional responses support and provide an updated, detailed and congruent version of early models assuming a general RH dominance for emotions.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Guido Gainotti

References

Ahern

Schwartz

. 1979. Differential lateralization for positive versus negative emotion. Neuropsychologia 17:693–8.

Allen

JJB

Keune

Schönenberg

Nusslock

. 2018. Frontal EEG alpha asymmetry and emotion: from neural underpinnings and methodological considerations to psychopathology and social cognition. Psychophysiology 55(e1). doi: 10.1111/psyp.13028.

Allman

Tetreault

Hakeem

Manaye

Semendeferi

Erwin

, and others. 2010. The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct 214:495–517.

Aron

Robbins

Poldrack

. 2004. Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–7.

Aron

Robbins

Poldrack

. 2014. Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci 18:177–85.

Asthana

Mandal

. 1998. Hemifacial asymmetry in emotion expression. Behav Modif 22:177–83.

Asthana

Mandal

. 2001. Visual-field bias in the judgment of facial expression of emotion. J Gen Psychol 128:21–9.

Boes

Bechara

Tranel

Anderson

Richman

Nopoulos

2009. Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys. Soc Cogn Affect Neurosc 4:1–9.

Borod

Bloom

Brickman

Nakhutina

Curko

. 2002. Emotional processing deficits in individuals with unilateral brain damage. Appl Neuropsychol 9:23–36.

10.

Borod

Haywood

Koff

1997. Neuropsychological aspects of facial asymmetry during emotional expression: a review of the normal adult literature. Neuropsychol Rev 7:41–60.

11.

Borod

Kent

Koff

Martin

Alpert

1988. Facial asymmetry while posing positive and negative emotions: support for the right hemisphere hypothesis. Neuropsychologia 26:759–64.

12.

Borod

Koff

Lorch

Nicholas

1986. The expression and perception of facial emotion in brain-damaged patients. Neuropsychologia 24:169–80.

13.

Borod

Zgaljardic

Tabert

Koff

2001. Asymmetries of emotional perception and expression in normal adults. In: Gainotti

, editor. Emotional behavior and its disorders ( Boller

Grafman

, editors. Handbook of neuropsychology, 2nd edition, Vol. 5), Amsterdam: Elsevier. p. 181–205.

14.

Broca

1865. Sur la faculté du langage articulé. Bull Soc Antropol Paris 6:377–93.

15.

Bryden

. 1982. Laterality: Hemispheric specialization in intact brain, New York: Academic Press.

16.

Buchtel

Campari

DeRisio

Rota

1978. Hemispheric differences in discriminative reaction time to facial expression. Ital J Psychol 5:159–69.

17.

Carmon

Nachshon

1973. Ear asymmetry in perception of emotional non-verbal stimuli. Acta Psychol (Amst) 37:351–7.

18.

Carver

Harmon-Jones

2009. Anger is an approach-related affect: evidence and implications. Psychol Bull 135:183–204.

19.

Coad

Postans

Hodgetts

Muhlert

Graham

Lawrence

, 2017. Structural connections support emotional connections: uncinate fasciculus microstructure is related to the ability to decode facial emotion expressions. Neuropsychologia. Epub Nov 6. doi:10.1016/j.neuropsychologia.2017.11.006.

20.

Craig

. 2005. Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–71.

21.

Craig

. 2009. How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70.

22.

Craig

. 2010. The sentient self. Brain Struct Funct 214:563–77.

23.

Craig

. 2011. Significance of the insula for the evolution of human awareness of feelings from the body. Ann N Y Acad Sci 1225:72–82.

24.

Critchley

Wiens

Rotshtein

Ohman

Dolan

. 2004. Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–95.

25.

Darwin

. 1872. The expression of the emotions in man and animals. 1st edition. London: John Murray.

26.

Davidson

. 1983. Hemispheric specialization for cognition and affect. In: Gale

Edwards

, editors. Physiological correlates of human behavior. London: Academic Press. p. 203–216.

27.

Davidson

. 1992. Anterior cerebral asymmetry and the nature of emotion. Brain Cogn 20:125–51.

28.

Davidson

. 1998. Affective style and affective disorders: perspectives from affective neuroscience. Cogn Emot 12:307–30.

29.

Davidson

Fox

. 1982. Asymmetrical brain activity discriminates between positive and negative stimuli in human infants. Science 218:1235–7.

30.

Davidson

Schwartz

Saron

Bennett

Goleman

. 1979. Frontal versus parietal EEG asymmetry during positive and negative affect. Psychophysiology 16:202–3.

31.

Dax

. 1865. Lésions de la moitié gauche de l’encéphale coincidant avec l’oubli ders signes de la pensée (read at the Meridional Congress held in Montpellier in 1836). Gazette Ebdomadaire Medico Chirurgical 2:259–60.

32.

Dopson

Beckwith

Tucker

Bullard-Bates

1984. Asymmetry of facial expression in spontaneous emotion. Cortex 20:243–52.

33.

Drevets

Raichle

. 1998. Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: implications for interactions between cognition and emotion. Cogn Emot 12:353–85.

34.

Duda

Brown

1984. Lateral asymmetry of positive and negative emotions. Cortex. 20:253–61.

35.

Ekman

. 1977. Facial Expression. In: Siegman

Feldstein

editors. Nonverbal communication and behavior. Hillsdale, NJ: Erlbaum. p. 97–126.

36.

Ekman

1984. Expression and the nature of emotions. In: Scherer

Ekman

, editors. Approaches to emotion. Hillsdale, NJ: Erlbaum. p. 319–44.

37.

Etcoff

. 1986. The neuropsychology of emotional expression. In: Goldstein

Tarter

, editors. Advances in clinical neuropsychology. New York: Plenum Press. p. 127–79.

38.

Frijda

. 1986. The emotions. Cambridge, UK: Cambridge University Press.

39.

Fusar-Poli

Piacentino

Carletti

Allen

Landi

Abbamonte

, and others. 2009. Laterality effect on emotional faces processing: ALE meta-analysis of evidence. Neurosci Lett 452:262–7.

40.

Gainotti

. 1969. Réaction “catastrophiques” et manifestations d’indifferénce au cours des atteintes cérébrales. Neuropsychologia 7:195–204.

41.

Gainotti

. 1972. Emotional behavior and hemispheric side of the lesion. Cortex 8:41–55.

42.

Gainotti

. 1996. Lateralization of brain mechanisms underlying automatic and controlled forms of spatial orienting of attention. Neurosci Biobehav Rev 20:617–22.

43.

Gainotti

. 2000. Neuropsychological theories of emotion. In: Borod

editor. The neuropsychology of emotion. New York: Oxford University Press. p. 214–236.

44.

Gainotti

. 2001. Components and levels of emotion disrupted in patients with unilateral brain damage. In: Gainotti

editor. Emotional behavior and its disorders ( Boller

Grafman

. editors. Handbook of neuropsychology. 2nd Edition, Vol. 5). Amsterdam: Elsevier. p. 161–80.

45.

Gainotti

2005. Emotions, unconscious processes and the right hemisphere. Neuro-Psychoanalysis 7:71–81.

46.

Gainotti

. 2007a. Face familiarity feelings, the right temporal lobe and the possibile underlying neural mechanisms. Brain Res Rev 56:214–35.

47.

Gainotti

. 2007b. Different patterns of famous people recognition disorders in patients with right and left anterior temporal lesions: a systematic review. Neuropsychologia 45:1591–607.

48.

Gainotti

2012a. Unconscious processing of emotions and the right hemisphere. Neuropsychologia 50:205–18.

49.

Gainotti

. 2012b. The Format of conceptual representations disrupted in semantic dementia: a position paper. Cortex 48:521–9.

50.

Gainotti

. 2015. Is the difference between right and left ATLs due to the distinction between general and social cognition or between verbal and non-verbal representations? Neurosci Biobehav Rev 51:296–312.

51.

Gainotti

Caltagirone

Zoccolotti

1993. Left/right and cortical/subcortical dichotomies in the neuropsychological study of human emotions. Cogn Emot 7:71–93.

52.

Gläscher

Adolphs

2003. Processing of the arousal of subliminal and supraliminal emotional stimuli by the human amygdala. J Neurosci 23:10274–82.

53.

Gray

Harrison

Wiens

Critchley

. 2007. Modulation of emotional appraisal by false physiological feedback during fMRI. PLoS One 2:e546. doi.org/10.1371/journal.pone.0000546

54.

Haggard

Parkinson

. 1971. Stimulus and task factors as determinants of ear advantages. Q J Exp Psychol 23:168–77.

55.

Heilman

Schwartz

Watson

. 1978. Hypoarousal in patients with the neglect syndrome and emotional indifference. Neurology 28:229–32.

56.

Heller

Levy

1981. Perception and expression of emotion in right-handers and left-handers. Neuropsychologia 19:263–72.

57.

Hugdahl

Iversen

Johnsen

. 1993. Laterality for facial expressions: does the sex of the subject interact with the sex of the stimulus face? Cortex 29:325–31.

58.

Hung

Smith

Bayl

Mills

Cheyne

Taylor

. 2010. Unattended emotional faces elicit early lateralized amygdala-frontal and fusiform activations. Neuroimage 50:727–33.

59.

Izard

. 1977. Human emotions. New York: Plenum Press.

60.

Killgore

Yurgelun-Todd

. 2007. The right-hemisphere and valence hypotheses: could they both be right (and sometimes left)? Soc Cogn Affect Neurosci 2:240–50.

61.

Kinsbourne

Bemporad

1984. Lateralization of emotion: a model and the evidence. In: Fox

Davidson

, editors. The psychobiology of affective development. Hillsdale, NJ: Erlbaum.

62.

Ladavas

Umiltà

Ricci-Bitti

. 1980. Evidence for sex differences in right-hemisphere dominance for emotions. Neuropsychologia 18:361–6.

63.

Landis

Assal

Perret

1979. Opposite cerebral hemispheric superiorities for visual associative processing of emotional facial expressions and objects. Nature 278:739–40.

64.

LeDoux

. 1996. The emotional brain. New York: Simon & Schuster.

65.

Levenson

Sturm

Haase

. (2014). Emotional and behavioral symptoms in neurodegenerative disease: a model for studying the neural bases of psychopathology. Annu Rev Clin Psychol 10:581–606.

66.

Leventhal

. 1974. Emotions: a basic problem for social psychology: classic and contemporary integrations. Chicago, IL: McNally.

67.

Leventhal

. 1987. A perceptual motor theory of emotion. In: Berkowitz

editor. Advances in experimental social psychology, Vol. 17. New York: Academic Press, p. 117–82.

68.

Ley

Bryden

. 1982. A dissociation of right and left hemispheric effects for recognizing emotional tone and verbal content. Brain Cogn 1:3–9.

69.

Mandal

Ambady

2004. Laterality of facial expressions of emotion: universal and culture-specific influences. Behav Neurol 15:23–34.

70.

Mandal

Asthana

Tandon

. 1993. Judgement of facial expression of emotion in unilateral brain-damaged patients. Arch Clin Neuropsychol 8:171–83.

71.

Mandal

Singh

. 1990. Lateral asymmetry in identification and expression of facial emotions. Cogn Emot 4:61–70.

72.

Moreno

Borod

Welkowitz

Alpert

1990. Lateralization for the expression and perception of facial emotion as a function of age. Neuropsychologia 28:199–209.

73.

Morris

Ohman

Dolan

. 1998. Conscious and unconscious emotional learning in the human amygdala. Nature 393:467–70.

74.

Morris

Ohman

Dolan

. 1999. A subcortical pathway to the right amygdala mediating “unseen” fear. Proc Natl Acad Sci U S A 96:1680–5.

75.

Morrow

Vrtunski

Kim

Boller

1981. Arousal responses to emotional stimuli and laterality of lesion. Neuropsychologia 19:65–71.

76.

Moscovitch

Olds

1982. Asymmetries in spontaneous facial expressions and their possible relation to hemispheric specialization. Neuropsychologia 20:71–81.

77.

Natale

Gur

. 1983. Hemispheric asymmetries in processing emotional expressions. Neuropsychologia 21:555–65.

78.

Nicholls

Wolfgang

Clode

Lindell

. 2002. The effect of left and right poses on the expression of facial emotion. Neuropsychologia 40:1662–5.

79.

Nomura

Ohira

Haneda

Iidaka

Sadato

Okada

, and others. 2004. Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. Neuroimage 21:352–63.

80.

Oatley

Johnson-Laird

1987. Toward a cognitive theory of emotions. Cogn Emot 1:29–50.

81.

Panksepp

. 1989. The neurobiology of emotions: of animal brains and human feelings. In: Manstead

Wagner

editors. Handbook of social psychophysiology. Chichester, UK: Wiley. p. 5–26.

82.

Papinutto

Galantucci

Mandelli

Gesierich

Jovicich

Caverzasi

, and others. 2016. Structural connectivity of the human anterior temporal lobe: a diffusion magnetic resonance imaging study. Hum Brain Mapp 37:2210–22.

83.

Plutchik

. 1980. Emotion: a psychobioevolutionary synthesis. New York: Harper & Row.

84.

Reuter-Lorenz

Davidson

. 1981. Differential contribution of the two cerebral hemispheres to the perception of happy and sad faces. Neuropsychologia 19:609–13.

85.

Reuter-Lorenz

Givis

Moscovitch

1983. Hemispheric specialization and the perception of emotion: evidence from right–handers and from inverted and noninverted left handers. Neuropsychologia 21:687–92.

86.

Reznik

Allen

JJB

. 2018. Frontal asymmetry as a mediator and moderator of emotion: an updated review. Psychophysiology 55(1). doi:10.1111/psyp.12965.

87.

Rodway

Wright

Hardie

2003. The valence-specific laterality effect in free viewing conditions: the influence of sex, handedness, and response bias. Brain Cogn 53:452–63.

88.

Ross

. 1981. The aprosodias. Functional-anatomic organization of the affective components of language in the right hemisphere. Arch Neurol 38:561–9.

89.

Ross

. 1984. Right’s hemisphere role in language, affective behaviour and emotion. Trends Neurosci 7:342–6.

90.

Ross

Monnot

2007. Neurology of affective prosody and its functional-anatomic organization in right hemisphere. Brain Lang 104:51–74.

91.

Ross

Pulusu

. 2013. Posed versus spontaneous facial expressions are modulated by opposite cerebral hemispheres. Cortex 49:1280–91.

92.

Rossi

Rosadini

1967. Experimental analysis of cerebral dominance in man. In: Millikan

Darley

. editors. Brain mechanisms underlying speech and language. New York: Grune & Stratton. p. 167–74.

93.

Russell

Barrett

1999. Core affect, prototypical emotional episodes, and other things called emotion: dissecting the elephant. J Pers Soc Psychol 76:805–19.

94.

Sackeim

Grega

. 1987. Perceiver bias in the processing of deliberately asymmetric emotional expressions. Brain Cogn 6:464–73.

95.

Sackeim

Gur

. 1978. Lateral asymmetry in intensity of emotional expression, Neuropsychologia 16:473–81.

96.

Schiff

Lamon

1989. Inducing emotion by unilateral contraction of facial muscles: a new look at hemispheric specialization and the experience of emotion. Neuropsychologia 27:923–35.

97.

Shamay-Tsoory

Tomer

Berger

Aharon-Peretz

2003. Characterization of empathy deficits following prefrontal brain damage: the role of the right ventromedial prefrontal cortex. J Cogn Neurosci 15:324–37.

98.

Shamay-Tsoory

Tomer

Berger

Goldsher

Aharon-Peretz

2005. Impaired “affective theory of mind” is associated with right ventromedial prefrontal damage. Cogn Behav Neurol 18:55–67.

99.

Spielberg

Stewart

Levin

Miller

Heller

2008. Prefrontal cortex, emotion, and approach/withdrawal motivation. Soc Pers Psychol Compass 2:135–53.

100.

Strauss

Moscovitch

1981. Perception of facial expression. Brain Lang 13:308–32.

101.

Suberi

McKeever

. 1977. Differential right hemispheric memory storage of emotional and non-emotional faces. Neuropsychologia 15:757–68.

102.

Tamietto

de Gelder

2010. Neural bases of the non-conscious perception of emotional signals. Nat Rev Neurosci 11:697–709.

103.

Terzian

Cecotto

1959. Su un nuovo metodo per la determinazione e lo studio della dominanza emisferica. Giorn Psichiatr Neuropatol 87:889–924.

104.

Tranel

Bechara

Denburg

. 2002. Asymmetric functional roles of right and left ventromedial prefrontal cortices in social conduct, decision-making, and emotional processing. Cortex 38:589–612.

105.

Vingerhoets

Berckmoes

Stroobant

2003. Cerebral hemodynamics during discrimination of prosodic and semantic emotion in speech studied by transcranial doppler ultrasonography. Neuropsychology 17:93–9.

106.

Voyer

Russell

McKenna

2002. On the reliability of laterality effects in a dichotic emotion recognition task. J Clin Exp Neuropsychol 24:605–14.

107.

Wager

Phan

Liberzon

Taylor

. 2003. Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. Neuroimage 19:513–31.

108.

Williams

Das

Liddell

Kemp

Rennie

Gordon

2006. Mode of functional connectivity in amygdala pathways dissociates level of awareness for signals of fear. J Neurosci 26:9264–71.

109.

Wittling

1990. Psychophysiological correlates of human brain asymmetry: blood pressure changes during lateralized presentation of an emotionally laden film. Neuropsychologia 28:457–70.

110.

Wittling

Roschmann

1993. Emotion-related hemispheric asymmetry: subjective emotional response to laterally presented films. Cortex 29:431–48.

111.

Wright

Martis

Schwartz

Shin

Fischer

McMullin

, and others. 2003. Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex. Neuroimage 18:660–9.

112.

Wylie

Goodale

. 1988. Left-sided oral asymmetries in spontaneous but not posed smiles. Neuropsychologia 26:823–32.

113.

Xue

Levin

Bechara

2010. The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50:709–16.

114.

Zald

Andreotti

2010. Neuropsychological assessment of the orbital and ventromedial prefrontal cortex. Neuropsychologia 48:3377–91.

115.

Zoccolotti

Caltagirone

Benedetti

Gainotti

1986. Perturbation des réponses végétatives aux stimuli émotionnels au cours des lésions hémisphériques unilatérales. Encephale 12:263–8.

116.

Zoccolotti

Scabini

Violani

1982. Electrodermal responses in patients with unilateral brain damage. J Clin Neuropsychol 4:143–50.