Mainly Visual Aspects of Emotional Laterality in Cognitively Developed and Highly Social Mammals-A Systematic Review.

Several studies have shown that emotions are asymmetrically represented in the human brain and have proposed three main models (the 'right hemisphere hypothesis', the 'approach-withdrawal hypothesis' and the 'valence hypothesis') that give different accounts of this emotional laterality. Furthermore, in recent years, many investigations have suggested that a similar emotional laterality may also exist in different animal taxa. However, results of a previous systematic review of emotional laterality in non-human primates have shown that some of these studies might be criticized from the methodological point of view and support only in part the hypothesis of a continuum in emotional laterality across vertebrates. The aim of the present review therefore consisted in trying to expand this survey to other cognitively developed and highly social mammals, focusing attention on mainly visual aspects of emotional laterality, in studies conducted on the animal categories of horses, elephants, dolphins and whales. The 35 studies included in the review took into account three aspects of mainly visual emotional laterality, namely: (a) visual asymmetries for positive/familiar vs. negative/novel stimuli; (b) lateral position preference in mother-offspring or other affiliative interactions; (c) lateral position preference in antagonistic interactions. In agreement with data obtained from human studies that have evaluated comprehension or expression of emotions at the facial or vocal level, these results suggest that a general but graded right-hemisphere prevalence in the processing of emotions can be found at the visual level in cognitively developed non-primate social mammals. Some methodological problems and some implications of these results for human psychopathology are briefly discussed.

Testing of behavioural asymmetries as markers for brain lateralization of emotional states in pet dogs: A critical review.

Domestic dogs (Canis familiaris) hold a unique position in human society, particularly in their role as social companions; as such, it is important to understand their emotional lives. There has been growing interest in studying behavioural biases in dogs as indirect markers (reflecting lateralized brain activity) of their emotional states. In this paper, we not only review the previous literature on emotion-related behavioural lateralization in dogs, but also propose and apply the concept of evidential weight to previous research. This allows us to examine different hypotheses about emotion-related brain asymmetries (i.e., Right-Hemisphere-, Valence-, Approach-Withdrawal-Hypothesis) on the basis of a "likelihood-ist" concept of evidence. We argue that previous studies have not been able to discriminate well between competing hypotheses and tended to focus on confirmation bias than critically assess different hypotheses; as such there is a strong case for more systematic investigation to pull these theories apart. We present the areas for future research and explain their importance for understanding the emotional lives of dogs.

Ewww-Investigating the neural basis of disgust in response to naturalistic and pictorial nauseating stimuli.

Emotion induction in psychological and neuroscientific research has been mostly done by presenting participants with picture or film material. However, it is debatable whether this passive approach to emotion induction results in an affective state comparable to real-life emotions, and if the neural correlates of emotion processing are ecologically valid. To investigate the appropriateness of pictures for the induction of emotions, we presented 56 participants in a within-subjects design with naturalistic disgusting and neutral stimuli as well as with pictures of said stimulus material while recording continuous EEG data. We calculated asymmetry indices (AIs) for alpha power as an index of emotion processing and emotion regulation at the F3/4, F5/6, F7/8, and O1/2 electrode pairs. Participants reported higher disgust ratings for disgusting naturalistic compared to disgusting pictorial stimuli. Investigating changes in the EEG signal in participants with a pronounced disgust response (n = 38), we found smaller AIs for naturalistic stimuli compared to pictures. Moreover, in this disgusted sub-sample, there were smaller AIs in response to naturalistic disgusting stimuli compared to pictorial disgusting and neutral stimuli at the O1/2 electrode pair indicating stronger activation of the right relative to the left hemisphere by naturalistic stimuli. As the right hemisphere has been shown to display dominance in processing negative and withdrawal-associated emotions, this might indicate that naturalistic stimuli are more appropriate for the induction of emotions than picture stimuli. To improve the validity of results from emotion induction, future research should incorporate stimulus material that is as naturalistic as possible.

Recognition of musical emotions and their perceived intensity after unilateral brain damage.

For the hemispheric laterality of emotion processing in the brain, two competing hypotheses are currently still debated. The first hypothesis suggests a greater involvement of the right hemisphere in emotion perception whereas the second hypothesis suggests different involvements of each hemisphere as a function of the valence of the emotion. These hypotheses are based on findings for facial and prosodic emotion perception. Investigating emotion perception for other stimuli, such as music, should provide further insight and potentially help to disentangle between these two hypotheses. The present study investigated musical emotion perception in patients with unilateral right brain damage (RBD, n = 16) or left brain damage (LBD, n = 16), as well as in matched healthy comparison participants (n = 28). The experimental task required explicit recognition of musical emotions as well as ratings on the perceived intensity of the emotion. Compared to matched comparison participants, musical emotion recognition was impaired only in LBD participants, suggesting a potential specificity of the left hemisphere for explicit emotion recognition in musical material. In contrast, intensity ratings of musical emotions revealed that RBD patients underestimated the intensity of negative emotions compared to positive emotions, while LBD patients and comparisons did not show this pattern. To control for a potential generalized emotion deficit for other types of stimuli, we also tested facial emotion recognition in the same patients and their matched healthy comparisons. This revealed that emotion recognition after brain damage might depend on the stimulus category or modality used. These results are in line with the hypothesis of a deficit of emotion perception depending on lesion laterality and valence in brain-damaged participants. The present findings provide critical information to disentangle the currently debated competing hypotheses and thus allow for a better characterization of the involvement of each hemisphere for explicit emotion recognition and their perceived intensity.

How Target Animacy Affects Manual Laterality in Hylobatidae: The First Evidence in Northern White-Cheeked Gibbons (Nomascus leucogenys).

Our study presents the first evidence on how target animacy impacts on manual laterality in the Hylobatidae and contributes to filling the knowledge gap between monkeys and great apes in primate evolution of emotional lateralization. Eleven captive individuals of northern white-cheeked gibbons (Nomascus leucogenys) were chosen as focal subjects. There were significantly more ambipreferent individuals than left/right-handed individuals for both inanimate (χ2(1, n = 11) = 7.364, p = 0.007) and animate (χ2(1, n = 11) = 4.455, p = 0.035) targets, meaning no significant group-level hand preference. The right hand was more frequently used than the left hand for inanimate targets whereas the left hand was more frequently used than the right hand for animate targets, although the interaction between target animacy and hand use was not significant (proportion: F1, 10 = 0.283, p = 0.607; rate: F1, 10 = 0.228, p = 0.643). Our findings in N. leucogenys could not fully support either the tool use theory or the right hemisphere hypothesis.

The Role of the Right Hemisphere in Emotional and Behavioral Disorders of Patients With Frontotemporal Lobar Degeneration: An Updated Review.

Background: Two main models have been advanced to explain the asymmetries observed in the representation and processing of emotions. The first model, labeled "the right hemisphere hypothesis," assumes a general dominance of the right hemisphere for all emotions, regardless of affective valence. The second model, named "the valence hypothesis," assumes an opposite dominance of the left hemisphere for positive emotions and the right hemisphere for negative emotions. Patients with frontotemporal lobar degeneration (FTLD) could contribute to clarifying this issue, because disorders of emotional and social behavior are very common in FTLD and because atrophy, which affects the antero-ventral part of the frontal and temporal lobes, can be clearly asymmetric in the early stages of this disease. Objective: The main scope of the present review therefore consists of evaluating if results of investigations conducted on emotional and behavioral disorders of patients with right and left FTLD, support the "right hemisphere" or the "valence" hypothesis. Method: A thorough review of behavioral and emotional disorders in FTLD patients, found that 177 possible studies, but only 32 papers met the requested criteria for inclusion in our review. Results: Almost all (25 out of 26) studies were relevant with respect to the "right hemisphere hypothesis" and supported the assumption of a general dominance of the right hemisphere for emotional functions, whereas only one of the six investigations were relevant with respect to the "valence hypothesis" and were in part consistent with this hypothesis, though these are also open to interpretation in terms of the "right hemisphere" hypothesis. Conclusions: This study, therefore, clearly supports the model of a general dominance of the right hemisphere for all emotions, regardless of affective valence.

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

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.

A historical review of investigations on laterality of emotions in the human brain.

Different models of emotional lateralization, advanced since the first clinical observations raised this issue, will be reviewed following their historical progression. The clinical investigations that have suggested a general dominance of the right hemisphere for all kinds of emotions and the experimental studies that have proposed a different hemispheric specialization for positive vs. negative emotions (valence hypothesis) or for approach vs. withdrawal tendencies (motivational hypothesis) will be reviewed first and extensively. This historical review will be followed by a short discussion of recent anatomo-clinical and activation studies that have investigated (a) emotional and behavioral disorders of patients with asymmetrical forms of fronto-temporal degeneration and (b) laterality effects in specific brain structures (amygdala, ventro-medial prefrontal cortex, and anterior insula) playing a critical role in different components of emotions. Overall, these studies support the hypothesis of a right hemisphere dominance for all components of the emotional system.

Transcranial random noise stimulation (tRNS) over prefrontal cortex does not influence the evaluation of facial emotions.

Cerebral asymmetries for emotion processing are controversial, the right hemisphere being considered either superior in the recognition of all emotions, or superior in the recognition of negative emotions (together with the left-hemispheric superiority for positive emotions). In a number of previous studies, tDCS was applied on the left/right prefrontal cortex (PFC) in order to disentangle this issue, but the results remain controversial. We applied hf-tRNS/sham stimulation over the left/right PFC, during the presentation of neutral, angry and happy faces presented as broadband images (supraliminal condition), and as "hybrid" stimuli in which an emotional face in low spatial frequency is superimposed to the neutral expression of the same individual in high spatial frequency (subliminal condition), during a friendliness evaluation task. The results showed that angry and happy unfiltered stimuli were judged as the most unfriendly and friendly, respectively. Importantly, we found that hf-tRNS applied over the left/right PFC did not influence friendliness evaluations for emotional faces.

Hemispheric asymmetries and emotions: Evidence from effective connectivity.

The Right Hemisphere Hypothesis (RHH) posits that the right hemisphere is specialized in processing all emotions; the Valence Hypothesis (VH) suggests a left/right-hemispheric specialization for positive/negative emotions, respectively. Behavioural, neuroimaging and physiological investigations alternatively support either the RHH or the VH, but connectivity analyses have been hardly exploited in this field. In the present study, unilateral and bilateral presentations of positive (happy) and negative (angry) emotional faces were used during electroencephalographic (EEG) recordings, and estimation of effective connectivity was performed using the Directed Transfer Function, to estimate causal influences between brain regions (Granger causality approach). The results show a strong pattern of connectivity among different frontal areas (orbitofrontal and dorsolateral prefrontal cortex), attentional network (frontal eye field, intraparietal sulcus), visual occipital areas and temporal sites, mainly lateralized in the right hemisphere for all emotions, in accordance with the RHH. Moreover, a stronger pattern of connectivity is evident when stimuli are presented in accordance with the VH (positive/negative emotions to the left/right hemisphere, respectively). Finally, the results suggest a crucial role of the right dorsolateral prefrontal cortex in a top-down regulation toward different areas involved in emotional processing. We conclude that the RHH and the VH are not mutually exclusive, but they seem to coexist during affective perception.

Effect of target animacy on hand preference in Sichuan snub-nosed monkeys (Rhinopithecus roxellana).

Twenty-eight captive Sichuan snub-nosed monkeys (Rhinopithecus roxellana) were involved in the current study. Many individuals showed handedness, with a modest tendency toward left-hand use especially for animate targets, although no group-level handedness was found. There was no significant gender difference in the direction and strength of hand preference for both targets. Females showed a significantly higher overall rate of actions toward animate targets than inanimate targets for both hands, whereas males displayed almost the reversed pattern. There were no significant interactions between lateral hand use and target animacy for either males or females. Most individuals showed rightward or leftward laterality shift trends between inanimate and animate targets. These findings to some extent support the existence of a potential trend concerning a categorical neural distinction between targets demanding functional manipulation (inanimate objects) and those demanding social manipulation (animate objects), even though specialized hand preference based on target animacy has not been fully established in this arboreal Old World monkey species.

A leftward bias however you look at it: Revisiting the emotional chimeric face task as a tool for measuring emotion lateralization.

Left hemiface biases observed within the Emotional Chimeric Face Task (ECFT) support emotional face perception models whereby all expressions are preferentially processed by the right hemisphere. However, previous research using this task has not considered that the visible midline between hemifaces might engage atypical facial emotion processing strategies in upright or inverted conditions, nor controlled for left visual field (thus right hemispheric) visuospatial attention biases. This study used novel emotional chimeric faces (blended at the midline) to examine laterality biases for all basic emotions. Left hemiface biases were demonstrated across all emotional expressions and were reduced, but not reversed, for inverted faces. The ECFT bias in upright faces was significantly increased in participants with a large attention bias. These results support the theory that left hemiface biases reflect a genuine bias in emotional face processing, and this bias can interact with attention processes similarly localized in the right hemisphere.

Asymmetries in the production of self-directed behavior by chimpanzees and gorillas during a computerized cognitive test.

Self-directed behaviors (SDBs) are a commonly used behavioral indicator of arousal in nonhuman primates. Experimental manipulations, designed to increase arousal and uncertainty, have been used to elicit SDB production in primates. Beyond measuring rates of SDB production, researchers have also recorded their lateralized production by primates, thought to reflect laterality of hemispheric brain control and response to emotion. Although a handful of such studies exist, all have been conducted with chimpanzees. Expanding on this line of inquiry, we tested both chimpanzees (N = 3) and gorillas (N = 3) in a serial learning task presented on a touchscreen interface that incorporated both EASY (two-item list) and HARD (four-item list) versions of the task. Although SDB production by the apes did not differ across the two levels of task complexity, both species produced higher rates of SDB when they made an error, regardless of task difficulty. Furthermore, the apes made more SDB with the left hand-directed to the right side of their body (contralateral SDB) and left side of their body (ipsilateral SDB)-when they made an incorrect response. There was no difference in the rate of SDB produced with the right hand across correct compared to incorrect trials. The apes' responses reflect previous reports that show humans are quicker at selecting negative emotional stimuli when using their left, compared to their right, hand (the reverse is true for positive stimuli). However, previous work has shown that chimpanzees are more likely to produce (contralateral) SDB with their right hand when aroused and so we discuss our results in relation to these findings and consider how they relate to the 'right hemisphere' and 'valence' models of emotional processing in apes.

Right hemisphere or valence hypothesis, or both? The processing of hybrid faces in the intact and callosotomized brain.

The valence hypothesis and the right hemisphere hypothesis in emotion processing have been alternatively supported. To better disentangle the two accounts, we carried out two studies, presenting healthy participants and an anterior callosotomized patient with 'hybrid faces', stimuli created by superimposing the low spatial frequencies of an emotional face to the high spatial frequencies of the same face in a neutral expression. In both studies we asked participants to judge the friendliness level of stimuli, which is an indirect measure of the processing of emotional information, despite this remaining "invisible". In Experiment 1 we presented hybrid faces in a divided visual field paradigm using different tachistoscopic presentation times; in Experiment 2 we presented hybrid chimeric faces in canonical view and upside-down. In Experiments 3 and 4 we tested a callosotomized patient, with spared splenium, in similar paradigms as those used in Experiments 1 and 2. Results from Experiments 1 and 3 were consistent with the valence hypothesis, whereas results of Experiments 2 and 4 were consistent with the right hemisphere hypothesis. This study confirms that the low spatial frequencies of emotional faces influence the social judgments of observers, even when seen for 28 ms (Experiment 1), possibly by means of configural analysis (Experiment 2). The possible roles of the cortical and subcortical emotional routes in these tasks are discussed in the light of the results obtained in the callosotomized patient. We propose that the right hemisphere and the valence accounts are not mutually exclusive, at least in the case of subliminal emotion processing.

Models of brain asymmetry in emotional processing

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.