Emotional and non-emotional facial behaviour in patients with unilateral brain damage.

Aspects of emotional facial expression (responsivity, appropriateness, intensity) were examined in brain-damaged adults with right or left hemisphere cerebrovascular lesions and in normal controls. Subjects were videotaped during experimental procedures designed to elicit emotional facial expression and non-emotional facial movement (paralysis, mobility, praxis). On tasks of emotional facial expression, patients with right hemisphere pathology were less responsive and less appropriate than patients with left hemisphere pathology or normal controls. These results corroborate other research findings that the right cerebral hemisphere is dominant for the expression of facial emotion. Both brain-damaged groups had substantial facial paralysis and impairment in muscular mobility on the hemiface contralateral to site of lesion, and the left brain-damaged group had bucco-facial apraxia. Performance measures of emotional expression and non-emotional movement were uncorrelated, suggesting a dissociation between these two systems of facial behaviour.     

The contribution of anterior and posterior regions of the right hemisphere to the recognition of emotional faces

To investigate the contribution of posterior and anterior parts of the right hemisphere (RH) to emotional facial recognition, we studied 11 participants with anterior strokes of the right hemisphere (ASRH), 16 patients with posterior strokes of the right hemisphere (PSRH), and 31 normal controls. All individuals were right-handed and nondemented. The ability to recognize emotional facial expressions was assessed by using Ekman and Friesen's (1976) Pictures of Facial Affect. Analysis revealed that both groups of patients presented with an impaired recognition of emotional faces. However, patients with PSRH were able to identify facial expressions better than participants with ASRH. In comparison to participants sustaining PSRH, patients with ASRH were particularly impaired on recognizing faces of negative valence. Thus, our results suggest that anterior parts of the RH seem to play an important role in the recognition of emotional facial expressions.     

Differential effects of lesions of the amygdala and prefrontal cortex on recognizing facial expressions of complex emotions

Humans can detect facial expressions of both simple, basic emotions and expressions reflecting more complex states of mind. The latter includes emotional expressions that regulate social interactions ("social expressions" such as looking hostile or friendly) and expressions that reflect the inner thought state of others ("cognitive expressions" such as looking pensive). To explore the neural substrate of this skill, we examined performance on a test of detection of such complex expressions in patients with lesions of the temporal lobe (n = 54) or frontal lobe (n = 31). Of the temporal group, 18 had unilateral focal lesions of the amygdala and of the frontal group, 14 patients had unilateral lesions of the ventromedial prefrontal cortex-two regions held to be pivotal in mediating social cognitive skills. Damage to either the left or right amygdala was associated with impairment in the recognition of both social and cognitive expressions, despite an intact ability to extract information relating to invariant physical attributes. Lesions to all of the right prefrontal cortex-not just the ventromedial portions-led to a specific deficit in recognizing complex social expressions with a negative valence. The deficit in the group with right prefrontal cortical damage may contribute to the disturbances in social behavior associated with such lesions. The results also suggest that the amygdala has a role in processing a wide range of emotional expressions.     

Spontaneous facial expression of emotions in brain-damaged patients

Spontaneous facial expression of emotion was studied in two groups of right (N = 23) and left (N = 39) brain-damaged patients and in a control group of normal subjects (N = 28). To elicit emotions four short movies, constructed to produce positive, negative or neutral emotional responses, were used. The method used to assess the facial expression of emotions was the Facial Action Coding System. Brain-damaged patients showed less facial responses to emotional stimuli than normal controls, but no difference was observed between subjects with right and left-sided lesions either with global or disaggregated data analyses, inconsistent with the hypothesis of a specialization of the right hemisphere for facial emotional expressions. An unexpected difference was observed in response to the unpleasant movie. Both normal controls and left brain-damaged patients often averted their gaze from the screen when unpleasant material was displayed, whereas right brain-damaged patients rarely showed gaze aversion. This finding suggests that the degree of emotional involvement or manner of coping with stressful input may be reduced as a result of right brain damage.     

Intact recognition of emotional prosody following amygdala damage.

Bilateral damage to the amygdala in a variety of animal species can impair emotional reactions to stimuli in several sensory modalities. Such damage in humans impairs visual recognition of emotion in facial expressions, but possible impairments in modalities other than vision have not been sufficiently explored. We examined two subjects with complete bilateral amygdala damage, and seven with unilateral amygdala damage, on a standardized task of emotional prosody recognition. The data were compared to those from 15 brain-damaged and from 14 normal control subjects. One of the bilateral amygdala subjects, whose lesions were restricted to the amygdala, was entirely normal in recognizing emotion in prosody on all tasks, the other, whose damage included substantial lesions also in extra-amygdalar structures, especially in right hemisphere, was normal on most, albeit not all, measures of emotional prosody recognition. We suggest that the human amygdala's role in recognizing emotion in prosody may not be as critical as it is for facial expressions, and that extra-amygdalar structures in right hemisphere may be more important for recognizing emotional prosody. It remains possible that recognition of emotion in classes of auditory stimuli other than prosody will require the amygdala.     

Perception of emotions from faces and voices following unilateral brain damage

The importance of the right hemisphere in emotion perception in general has been well documented but its precise role is disputed. We compared the performance of 30 right hemisphere damaged (RHD) patients, 30 left hemisphere damaged (LHD) patients, and 50 healthy controls on both facial and vocal affect perception tasks of specific emotions. Brain damaged subjects had a single episode cerebrovascular accident localised to one hemisphere. The results showed that right hemisphere patients were markedly impaired relative to left hemisphere and healthy controls on test performance: labelling and recognition of facial expressions and recognition of emotions conveyed by prosody. This pertained at the level of individual basic emotions, positive versus negative, and emotional expressions in general. The impairment remained highly significant despite covarying for the group's poorer accuracy on a neutral facial perception test and identification of neutral vocal expressions. The LHD group were only impaired relative to controls on facial emotion tasks when their performance was summed over all the emotion categories and before age and other cognitive factors were taken into account. However, on the prosody test the LHD patients showed significant impairment, performing mid-way between the right hemisphere patients and healthy comparison group. Recognition of positive emotional expressions was better than negative in all subjects, and was not relatively poorer in the LHD patients. Recognition of individual emotions in one modality correlated weakly with recognition in another, in all three groups. These data confirm the primacy of the right hemisphere in processing all emotional expressions across modalities--both positive and negative--but suggest that left hemisphere emotion processing is modality specific. It is possible that the left hemisphere has a particular role in the perception of emotion conveyed through meaningful speech.     

Event-related synchronization and desynchronization during affective processing: emergence of valence-related time-dependent hemispheric asymmetries in theta and upper alpha band

Event-related desynchronization (ERD) and synchronization (ERS) in the individually defined theta, alpha-1, alpha-2, and alpha-3 frequency bands were measured in 22 healthy subjects (Ss) in response to neutral (Neut), emotionally positive (Pos), and negative (Neg) IAPS stimuli. The 62-channel EEG, facial EMG and ECG were simultaneously recorded while subjects viewed sequentially presented pictures and subjectively rated them after each presentation. The obtained findings indicate that differences induced by pictures varying in emotional valence are associated mainly with increased theta and alpha-3 synchronization activity and anterior hemispheric asymmetries. In the anterior temporal leads theta ERS revealed a significant valence by hemisphere interaction showing relatively greater right hemisphere theta ERS for Neg and left hemisphere ERS for Pos stimuli in the time window of 100-700 ms post-stimulus, whereas in the alpha-3 band Neg stimuli induced lateralized time-dependent left hemisphere ERS increased in the time window of 800-1200 ms, were not observed for Neut and Pos stimuli. The obtained results along with earlier observations on EEG correlates of affective processing challenge the notion that affective anterior hemispheric asymmetries are mainly sensitive to wide alpha frequency band. Frequency and time dependence of anterior hemispheric asymmetries in emotional valence discrimination is emphasized.     

Orbitofrontal cortex lesions result in abnormal social judgements to emotional faces

Facial expressions of emotion display a wealth of important social information that we use to guide our social judgements. The aim of the current study was to investigate whether patients with orbitofrontal cortex (OFC) lesions exhibit an impaired ability to judge the approachability of emotional faces. Furthermore, we also intended to establish whether impaired approachability judgements provided to emotional faces emerged in the presence of preserved explicit facial expression recognition. Using non-parametric statistics, we found that patients with OFC lesions had a particular difficulty using negative facial expressions to guide approachability judgements, compared to healthy controls and patients with frontal lesions sparing the OFC. Importantly, this deficit arose in the absence of an explicit facial expression recognition deficit. In our sample of healthy controls, we also demonstrated that the capacity to recognise facial expressions was not significantly correlated with approachability judgements given to emotional faces. These results demonstrate that the integrity of the OFC is critical for the appropriate assessment of approachability from negatively valenced faces and this ability is functionally dissociable from the capacity to explicitly recognise facial expressions.     

The asymmetric lateralization of tactile extinction in patients with unilateral cerebral dysfunction

Two hundred and thirty-four patients with unilateral cerebral pathology and 175 control subjects were examined with a sensitive test for tactile extinction. Damage to the right hemisphere was associated with extinction slightly (but not significantly) more often than damage to the left hemisphere; the asymmetry may be due to selective exclusion of aphasics with damage to the left hemisphere. Extinction of the left side of the body, however, was significantly more common than of the right side; this asymmetry could not be accounted for by exclusion of untestable aphasics, but was a consequence of frequent ipsilateral (left side) extinction among the group with damage to the left hemisphere while the group with damage to the right hemisphere extinguished the contralateral (left) side almost exclusively. Although the hemispheres as a whole did not differ in their association with extinction, lesions in the right parietal lobe were significantly more effective in producing extinction than lesions in the left; in both cases the contralateral side of the body was affected. By contrast, lesions in the left frontal lobe were moderately but not significantly more effective in producing extinction than right frontal damage; in almost all these cases the left side of the body was affected, regardless of which frontal lobe was damaged. A relationship between extinction and pathology in the vicinity of the anterior callosum, as determined from CT scan and angiography, was found among the frontal cases. We propose an anatomical model to explain tactile extinction and its asymetric characteristics in the human. During the extinction tests a response mechanism in the left (speech) hemisphere bases its perceptual output on the relative strengths of two simultaneous sensory inputs. Damage at any point in the channel from the periphery to the response mechanism weakens one signal in comparison to the other, resulting in a response bias favouring the stronger stimulus. Tactile information from the left hand, after reaching the somatosensory zone in the right hemisphere, is transmitted to the left hemisphere by a diffuse, widespread network including the frontal lobes and the anterior callosum. This anatomical arrangement renders left-hand information more vulnerable to chance lesions than right-hand information, which has direct access to the response mechanism via a more compact projection system.     

Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia.

BACKGROUND: Prosopagnosia, the inability to recognize faces, is associated with medial occipitotemporal lesions, especially on the right. Functional imaging has revealed a focal region in the right fusiform gyrus activated specifically during face perception. OBJECTIVE: The study attempted to determine whether lesions of this region were associated with defects in face perception in patients with prosopagnosia. METHODS: Five patients with acquired prosopagnosia were tested. They were asked to discriminate faces in which the spatial configuration of features had been altered. This was contrasted with their discrimination of changes in feature color, an alteration that does not affect spatial relations. RESULTS: All four patients whose lesions included the right fusiform face area were severely impaired in discriminating changes in the spatial position of features. The one patient with anterior bilateral lesions was normal in this perceptual ability. For three of the five patients, accuracy was normal for changes in eye color. When subjects knew that only changes in mouth position would be shown, performance improved markedly in two of the four patients who were impaired in the initial test. CONCLUSION: Perception of facial configuration is impaired in patients with prosopagnosia whose lesions involve the right fusiform gyrus. This deficit is especially manifest when attention must be distributed across numerous facial elements. It does not occur with more anterior bilateral temporal lesions. Loss of this ability may contribute to the recognition defect in some forms of prosopagnosia.     

Effects of lesion variables and emotion type on the perception of facial emotion.

The purpose of this study was to consider the effects of valence, motoric direction (i.e., approach/withdrawal), and arousal on the perception of facial emotion in patients with unilateral cortical lesions. We also examined the influence of lesion side, site, and size on emotional perception. Subjects were 30 right-hemisphere-damaged (RHD) and 30 left-hemisphere-damaged (LHD) male patients with focal lesions restricted primarily to the frontal, temporal, or parietal lobe. Patient groups were comparable on demographic and clinical neurological variables. Subjects were tested for their ability to match photographs of four facial emotional expressions: happiness, sadness, fear, and anger. Overall, RHD patients were significantly more impaired than LHD patients in perceiving facial emotion. Lesion side, but not site, was associated with motoric direction and valence dimensions. RHD patients had specific deficits relative to LHD patients in processing negative and withdrawal emotions; there were no group differences for positive/approach emotions. Lesion size was not significantly correlated with accuracy of emotional perception.     

Lateralisation effect in comprehension of emotional facial expression: A comparison between EEG alpha band power and behavioural inhibition (BIS) and activation (BAS) systems

Asymmetry in comprehension of facial expression of emotions was explored in the present study by analysing alpha band variation within the right and left cortical sides. Second, the behavioural activation system (BAS) and behavioural inhibition system (BIS) were considered as an explicative factor to verify the effect of a motivational/emotional variable on alpha activity. A total of 19 participants looked at an ample range of facial expressions of emotions (anger, fear, surprise, disgust, happiness, sadness, and neutral) in random order. The results demonstrated that anterior frontal sites were more active than central and parietal sites in response to facial stimuli. Moreover, right and left side responses varied as a function of emotional types, with an increased right frontal activity for negative, aversive emotions vs an increased left response for positive emotion. Finally, whereas higher BIS participants generated more right hemisphere activation for some negative emotions (such as fear, anger, surprise, and disgust), BAS participants were more responsive to positive emotion (happiness) within the left hemisphere. Motivational significance of facial expressions was considered to elucidate cortical differences in participants' responses to emotional types.     

Primate phonation: Unilateral and bilateral cingulate lesion effects

Four juvenile Macaca mulatta were trained on a multiple schedule to perform discriminative vocalization and lever press tasks. Sequential unilateral and bilateral lesions of the anterior cingulate gyrus were made with testing of vocalization and lever press at each stage. Performance of the two behavioral tasks was assessed in terms of total responses, latency, efficiency and error index.Unilateral damage had a profound effect on vocal performance in one monkey. There was a significant deficit in total vocal responses and an increase of vocal response latency. No such impairment occurred from equivalent damage in the 3 remaining animals, despite comparable lesions. None of the 4 suffered changes in discriminative lever press following unilateral lesions.The second lesion (producing bilateral damage) had little further effect on the animal that exhibited an initial deficit from a unilateral insult. In contrast, this step in the remaining monkeys produced latency and total vocal response scores that approximated the scores obtained from the monkey with a single, unilateral hemisphere lesion.The evidence indicates there is lateral asymmetry in vocal mechanisms involving anterior cingulate cortex. This may be related to the hemisphere controlling the preferred hand. The principal effect of anterior cingulate damage involves impaired response initiation.     

Altered tonic and phasic cortisol secretion following unilateral stroke

Evidence is accumulating that cerebral laterality appears to be an important feature in the regulation of the stress response with the right hemisphere being closely linked to stress-regulatory systems, including the hypothalamic-pituitary-adrenal (HPA) axis. Although some animal and human data support this hypothesis, studies on brain damaged patients yet failed to substantiate laterality effects on cortisol secretion. The aim of this study was to examine whether unilateral stroke differentially affects tonic and phasic response characteristics of the HPA axis, and to evaluate the impact of intrahemispheric lesion location. Basal morning cortisol levels and phasic responses towards a mentally challenging task were examined in 32 stroke patients with left-sided (LH; n=18) or right-sided (RH; n=14) infarctions and 30 healthy controls matched for age and gender. Only LH, but not RH patients displayed increased morning cortisol levels when compared to controls. In contrast, phasic reactions were blunted in the combined patient group with RH patients showing the most distinct decline. More anterior located lesions were associated with reduced phasic, but not tonic cortisol measures. This relationship appeared to be particularly pronounced in RH patients. Results support the conclusion that the central regulation of cortisol secretion is under excitatory control of the right hemisphere and can be interpreted within a framework of asymmetrical regulation of the stress response. Left- and right-sided strokes may differentially affect response patterns of the HPA axis, a stress-regulatory system that is associated with effective protection against disease and external challenges.     

Do reward-processing deficits in schizophrenia-spectrum disorders promote cannabis use? An investigation of physiological response to natural rewards and drug cues

Background

Dysfunctional reward processing is present in individuals with schizophrenia-spectrum disorders (SSD) and may confer vulnerability to addiction. Our objective was to identify a deficit in patients with SSD on response to rewarding stimuli and determine whether this deficit predicts cannabis use.

Methods

We divided a group of patients with SSD and nonpsychotic controls into cannabis users and nonusers. Response to emotional and cannabis-associated visual stimuli was assessed using self-report, event-related potentials (using the late positive potential [LPP]), facial electromyography and skin-conductance response.

Results

Our sample comprised 35 patients with SSD and 35 nonpsychotic controls. Compared with controls, the patients with SSD showed blunted LPP response to pleasant stimuli (p = 0.003). Across measures, cannabis-using controls showed greater response to pleasant stimuli than to cannabis stimuli whereas cannabis-using patients showed little bias toward pleasant stimuli. Reduced LPP response to pleasant stimuli was predictive of more frequent subsequent cannabis use (β = −0.24, p = 0.034).

Limitations

It is not clear if the deficit associated with cannabis use is specific to rewarding stimuli or nonspecific to any kind of emotionally salient stimuli.

Conclusion

The LPP captures a reward-processing deficit in patients with SSD and shows potential as a biomarker for identifying patients at risk of heavy cannabis use.     

Severe behavioral complications following intracarotid sodium amobarbital injection: implications for hemispheric asymmetry of emotion

The intracarotid sodium amobarbital (ISA) procedure is effective in determining cerebral language dominance. However, severe emotional and behavioral reactions during ISA evaluation may invalidate the results or necessitate aborting the procedure. In an effort to identify patients at risk for behavioral complications, we reviewed 92 patients undergoing ISA evaluation and found five with severe changes in affect and behavior following amobarbital injection, ranging from prolonged coma to an extended confusional state. Severe behavioral disturbances were more likely to occur in patients with left frontal structural lesions upon injecting amobarbital into the right hemisphere. Analysis of patients with structural lesions of the anterior regions of the right hemisphere showed no evidence of similar behavioral complications. These findings suggest a special role for the left frontal region in the inhibition of affective expression and provide further evidence of the importance of right hemisphere mechanisms in emotion.     

Social and motivational functioning is not critically dependent on feedback of autonomic responses: neuropsychological evidence from patients with pure autonomic failure

Social, emotional and motivational behaviours are associated with production of automatic bodily responses. Re-representation in the brain through feedback of autonomic and skeletomuscular arousal is proposed to underlie “feeling states”. These influence emotional judgments and bias motivational decision-making and guide social interactions. Consistent with this hypothesis, dissocial behaviour and deficits on emotional and motivation tasks are associated with blunted bodily responses in patients with orbitofrontal brain lesions or developmental psychopathy. To determine the critical dependence of social and emotional behaviours on bodily responses mediated by the autonomic nervous system, we examined patients with pure autonomic failure (PAF), a peripheral denervation of autonomic neurons with onset in middle age.

Compared to healthy subjects, PAF patients were unimpaired on tests of motivational decision-making (Iowa Gambling Task), recognition of emotional facial expressions, Theory of Mind Tasks and tests of social cognition. Only on a test of emotional attribution, which is perhaps more sensitive to subjective feeling states, did PAF patients score worse than the comparison group, though there was no evidence that this deficit was specific to a discrete emotion and requires further validation.

These findings suggest that emotional and social functioning is not critically tied to on-going experience of autonomic arousal state, Acquisition of autonomic failure late in life may protect against maladaptive social behaviour through established behavioural responses that may be associated with central “as if” representations.     

Facial emotion recognition in myotonic dystrophy type 1 correlates with CTG repeat expansion

Objective

To investigate the ability of patients with myotonic dystrophy type 1 to recognise basic facial emotions. We also explored the relationship between facial emotion recognition, neuropsychological data, personality, and CTG repeat expansion data in the DM‐1 group.

Methods

In total, 50 patients with DM‐1 (28 women and 22 men) participated, with 41 healthy controls. Recognition of facial emotional expressions was assessed using photographs of basic emotions. A set of tests measured cognition and personality dimensions, and CTG repeat size was quantified in blood lymphocytes.

Results

Patients with DM‐1 showed impaired recognition of facial emotions compared with controls. A significant negative correlation was found between total score of emotion recognition in a forced choice task and CTG repeat size. Furthermore, specific cognitive functions (vocabulary, visuospatial construction ability, and speed) and personality dimensions (reward dependence and cooperativeness) correlated with scores on the forced choice emotion recognition task.

Conclusion

These findings revealed a CTG repeat dependent facial emotion recognition deficit in the DM‐1 group, which was associated with specific neuropsychological functions. Furthermore, a correlation was found between facial emotional recognition ability and personality dimensions associated with sociability. This adds a new clinically relevant dimension in the cognitive deficits associated with DM‐1.     

Stroke of bad luck?

We hypothesized that distinct acute right hemisphere lesions disrupt separate components of valuation and emotional response to winning and losing money and of emotional empathy in observing a partner win or lose money. We measured skin conductance response (SCR) and ratings of emotions when acute right hemisphere stroke patients or healthy controls won or lost money in roulette, or when they watched a partner win or lose. Our results showed that percentage of damage after stroke to right anterior insula and frontal operculum negatively correlated with both SCR to winning and losing and difference between rating wins versus losses.     

Brain responses to emotional stimuli in patients with amyotrophic lateral sclerosis (ALS)

Amyotrophic lateral sclerosis (ALS), a progressive motor neuron disease, affects movement and communication abilities and emotional processing. Subjective ratings of emotional stimuli depicting social interactions and facial expressions differed significantly between ALS patients and healthy controls in a previous study with a reduction of negative emotional valence (pleasantness) and lower subjective arousal (excitement) in ALS patients. In the present study, sixty similar emotional slides were presented to 13 ALS patients, 15 matched healthy controls and six tetraplegic patients. Subjective reports of valence and arousal as well as brain responses to the affective pictures using functional magnetic resonance imaging (fMRI) were measured. The picture series was presented twice with a 6-months interval to investigate effects of disease progression. ALS patients presented an increased brain response in the right supramarginal area and a reduced brain response in extrastriate visual areas at both measurements compared with healthy controls. Within the ALS patients' group a reduction of brain responses in the anterior insula at the follow-up was correlated with the subjective arousal. The reduced response in the anterior insula is tentatively interpreted as indicating reduced arousal during the course of the disease at the neural and behavioural level. The reduction of activity in extrastriate visual areas might be similarly interpreted. The increased brain response in the right supramarginal area of ALS patients might represent an altered sensitivity to social-emotional cues.