Subthalamic nucleus stimulation induces deficits in decoding emotional facial expressions in Parkinson's disease

BACKGROUND: Bilateral subthalamic nucleus (STN) stimulation is recognised as a treatment for parkinsonian patients with severe levodopa related motor complications. Although adverse effects are infrequent, some behavioural disturbances have been reported. OBJECTIVE: To investigate the consequences of STN stimulation on emotional information processing in Parkinson's disease by assessing the performance of an emotional facial expression (EFE) decoding task in a group of patients before and after surgery. METHODS: 12 non-demented patients with Parkinson's disease were studied. They were assessed one month before surgery and three months after. Their ability to decode EFEs was assessed using a standardised quantitative task. Overall cognitive function, executive function, visuospatial perception, depression, and anxiety were also measured. Twelve healthy controls were matched for age, sex, and duration of education. RESULTS: Before surgery, the patients showed no impairment in EFE decoding compared with the controls. Their overall cognitive status was preserved but they had a moderate dysexecutive syndrome. Three months after surgery, they had significant impairment of EFE decoding. This was not related to their overall cognitive status or to depression/anxiety scores. Visuospatial perception was not impaired. There was no change in the extent of the dysexecutive syndrome except for a reduction in phonemic word fluency. CONCLUSIONS: Bilateral STN stimulation disturbs negative emotional information processing in Parkinson's disease. The impairment appears specific and unrelated to certain secondary variables. This behavioural complication of STN may have implications for the patient's social life.     

Facial expression decoding in early Parkinson's disease

The ability to derive emotional and non-emotional information from unfamiliar, static faces was evaluated in 21 adults with idiopathic Parkinson's disease (PD) and 21 healthy control subjects. Participants' sensitivity to emotional expressions was comprehensively assessed in tasks of discrimination, identification, and rating of five basic emotions: happiness, (pleasant) surprise, anger, disgust, and sadness. Subjects also discriminated and identified faces according to underlying phonemic ("facial speech") cues and completed a neuropsychological test battery. Results uncovered limited evidence that the processing of emotional faces differed between the two groups in our various conditions, adding to recent arguments that these skills are frequently intact in non-demented adults with PD [R. Adolphs, R. Schul, D. Tranel, Intact recognition of facial emotion in Parkinson's disease, Neuropsychology 12 (1998) 253-258]. Patients could also accurately interpret facial speech cues and discriminate the identity of unfamiliar faces in a normal manner. There were some indications that basal ganglia pathology in PD contributed to selective difficulties recognizing facial expressions of disgust, consistent with a growing literature on this topic. Collectively, findings argue that abnormalities for face processing are not a consistent or generalized feature of medicated adults with mild-moderate PD, prompting discussion of issues that may be contributing to heterogeneity within this literature. Our results imply a more limited role for the basal ganglia in the processing of emotion from static faces relative to speech prosody, for which the same PD patients exhibited pronounced deficits in a parallel set of tasks [M.D. Pell, C. Leonard, Processing emotional tone from speech in Parkinson's disease: a role for the basal ganglia, Cogn. Affect. Behav. Neurosci. 3 (2003) 275-288]. These diverging patterns allow for the possibility that basal ganglia mechanisms are more engaged by temporally-encoded social information derived from cue sequences over time.     

Decoding emotional prosody in Parkinson's disease and its potential neuropsychological basis

Parkinson's disease patients may have difficulty decoding prosodic emotion cues. These data suggest that the basal ganglia are involved, but may reflect dorsolateral prefrontal cortex dysfunction. An auditory emotional n-back task and cognitive n-back task were administered to 33 patients and 33 older adult controls, as were an auditory emotional Stroop task and cognitive Stroop task. No deficit was observed on the emotion decoding tasks; this did not alter with increased frontal lobe load. However, on the cognitive tasks, patients performed worse than older adult controls, suggesting that cognitive deficits may be more prominent. The impact of frontal lobe dysfunction on prosodic emotion cue decoding may only become apparent once frontal lobe pathology rises above a threshold.     

Facial recognition in primary focal dystonia.

The basal ganglia seem to be involved in emotional processing. Primary dystonia is a movement disorder considered to result from basal ganglia dysfunction, and the aim of the present study was to investigate emotion recognition in patients with primary focal dystonia. Thirty-two patients with primary cranial (n=12) and cervical (n=20) dystonia were compared to 32 healthy controls matched for age, sex, and educational level on the facially expressed emotion labeling (FEEL) test, a computer-based tool measuring a person's ability to recognize facially expressed emotions. Patients with cognitive impairment or depression were excluded. None of the patients received medication with a possible cognitive side effect profile and only those with mild to moderate dystonia were included. Patients with primary dystonia showed isolated deficits in the recognition of disgust (P=0.007), while no differences between patients and controls were found with regard to the other emotions (fear, happiness, surprise, sadness, and anger). The findings of the present study add further evidence to the conception that dystonia is not only a motor but a complex basal ganglia disorder including selective emotion recognition disturbances.     

Intra‐ and inter‐network functional alterations in Parkinson's disease with mild cognitive impairment

Mild cognitive impairment (MCI) is prevalent in 15%–40% of Parkinson's disease (PD) patients at diagnosis. In this investigation, we study brain intra‐ and inter‐network alterations in resting state functional magnetic resonance imaging (rs‐fMRI) in recently diagnosed PD patients and characterise them as either cognitive normal (PD‐NC) or with MCI (PD‐MCI). Patients were divided into two groups, PD‐NC (N = 62) and PD‐MCI (N = 37) and for comparison, healthy controls (HC, N = 30) were also included. Intra‐ and inter‐network connectivity were investigated from participants’ rs‐fMRIs in 26 resting state networks (RSNs). Intra‐network differences were found between both patient groups and HCs for networks associated with motor control (motor cortex), spatial attention and visual perception. When comparing both PD‐NC and PD‐MCI, intra‐network alterations were found in RSNs related to attention, executive function and motor control (cerebellum). The inter‐network analysis revealed a hyper‐synchronisation between the basal ganglia network and the motor cortex in PD‐NC compared with HCs. When both patient groups were compared, intra‐network alterations in RSNs related to attention, motor control, visual perception and executive function were found. We also detected disease‐driven negative synchronisations and synchronisation shifts from positive to negative and vice versa in both patient groups compared with HCs. The hyper‐synchronisation between basal ganglia and motor cortical RSNs in PD and its synchronisation shift from negative to positive compared with HCs, suggest a compensatory response to basal dysfunction and altered basal‐cortical motor control in the resting state brain of PD patients. Hum Brain Mapp 38:1702–1715, 2017 . © 2016 Wiley Periodicals, Inc.     

Parkinson's disease and arithmetics: the role of executive functions

Brain imaging studies as well as neuropsychological case studies suggest an important role for basal ganglia in arithmetic processing. Aim of this study was to assess possible numerical deficits in PD and functional relations between numerical and other cognitive deficits. Fifteen non-demented patients with early PD (stable responders treated by l-dopa) were compared to 28 healthy age and education matched controls. Both groups underwent a neuropsychological assessment focussing on numerical abilities (quantity processing, arithmetic fact retrieval, complex mental and written calculation, transcoding, arithmetic set-shifting, calculation span), working memory and executive functions. Patients with PD showed deficits in complex mental calculation and calculation span tasks. Results of this study suggest that impairments in working memory as well as in executive functions, such as inhibition of interference, lead to secondary deficits in numerical processing. The study contributes to better understanding the specific cognitive deficits in early PD and the neurocognitive architecture of arithmetic processing.     

An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson's disease

Parkinson's disease (PD) is a neurodegenerative movement disorder presenting with subcortical pathology and characterized by motor deficits. However, as is frequently reported in the literature, patients with PD can also exhibit cognitive and behavioral (i.e., nonmotor) impairments, cognitive executive deficits and depression being the most prominent. Considerable attention has addressed the role that disruption to frontostriatal circuitry can play in mediating nonmotor dysfunction in PD. The three nonmotor frontostriatal circuits, which connect frontal cortical regions to the basal ganglia, originate from the dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex (ACC), and orbitofrontal cortex (OFC). The objective of the current study was to use our understanding of frontostriatal circuit function (via literature review) to categorize neuropsychological measures of cognitive and behavioral executive functions by circuit. To our knowledge, such an approach has not been previously attempted in the study of executive dysfunction in PD. Neuropsychological measures of executive functions and self-report behavioral inventories, categorized by circuit function, were administered to 32 nondemented patients with Parkinson's disease (NDPD) and to 29 demographically matched, healthy normal control participants (NC). Our findings revealed significant group differences for each circuit, with the PD group performing worse than the NC group. Among the patients with PD, indices of impairment were greater for tasks associated with DLPFC function than with OFC function. Further, only an index of DLPFC test performance was demonstrated to significantly discriminate individuals with and without PD. In conclusion, our findings suggest that nondemented patients with PD exhibit greater impairment on neuropsychological measures associated with DLPFC than with ACC or OFC circuit function.     

Deep brain stimulation of the subthalamic nucleus enhances emotional processing in Parkinson disease

BACKGROUND: High-frequency electrical stimulation of the subthalamic nucleus is a new and highly effective therapy for complications of long-term levodopa therapy and motor symptoms in advanced Parkinson disease (PD). Clinical observations indicate additional influence on emotional behavior. METHODS: Electrical stimulation of deep brain nuclei with pulse rates above 100 Hz provokes a reversible, lesioning-like effect. Here, the effect of deep brain stimulation of the subthalamic nucleus on emotional, cognitive, and motor performance in patients with PD (n = 12) was examined. The results were compared with the effects of a suprathreshold dose of levodopa intended to transiently restore striatal dopamine deficiency. Patients were tested during medication off/stimulation off (STIM OFF), medication off/stimulation on (STIM ON), and during the best motor state after taking levodopa without deep brain stimulation (MED). RESULTS: More positive self-reported mood and an enhanced mood induction effect as well as improvement in emotional memory during STIM ON were observed, while during STIM OFF, patients revealed reduced emotional performance. Comparable effects were revealed by STIM ON and MED. Cognitive performance was not affected by the different conditions and treatments. CONCLUSIONS: Deep brain stimulation of the subthalamic nucleus selectively enhanced affective processing and subjective well-being and seemed to be antidepressive. Levodopa and deep brain stimulation had similar effects on emotion. This finding may provide new clues about the neurobiologic bases of emotion and mood disorders, and it illustrates the important role of the basal ganglia and the dopaminergic system in emotional processing in addition to the well-known motor and cognitive functions.     

Dopaminergic influence on disturbed spatial discrimination in Parkinson's disease.

Various sensory symptoms and disturbed sensory perception are often observed in patients with idiopathic Parkinson's disease (PD). The basis of sensory disturbance in PD is unknown but possibly reflects a role for the basal ganglia in sensory processing. To investigate the relationship between the sensory dysfunction and dopaminergic deficiency in PD, we measured spatial discrimination using the Grating Orientation Task in 21 drug-naive patients with PD, before and after long-term antiparkinson therapy, and 25 age-matched healthy controls. The grating orientation threshold was significantly higher in patients (3.03 +/- 0.84) than controls (2.03 +/- 0.79). After 3 to 10 months of antiparkinson therapy, the grating orientation threshold was significantly lowered (2.66 +/- 0.84), although it was still higher than that in controls. Improvement in the patients' sensory function was significantly correlated with motor improvement (r = 0.44). These results suggest that sensory dysfunction in Parkinson's disease is related at least in part to the dopaminergic deficit.     

Effects of stimulus–response compatibility on inhibitory processes in Parkinson's disease

Parkinson's disease (PD) is a neurodegenerative basal ganglia disorder accompanied by deficits in cognitive functions. One important executive function is the inhibition of responses. Due to basal ganglia damage, processes related to the selection of response are also dysfunctional. However, the relevance of deficits in response selection to processes related to response inhibition in PD is not clear. In this study we examined these processes by means of event-related potentials (ERPs) in two Go/Nogo tasks. In one task the stimulus–response mapping was compatible and in the other task it was incompatible with the meaning of the stimuli. The behavioural results show that PD patients were unaffected in the compatible response inhibition task but encountered problems in the incompatible one. In the ERPs the N2, generally reflecting response selection, was delayed for the PD compared to the control group. This suggests that response selection is delayed in PD. Moreover, the N2 was specifically enhanced in Nogo trials. This indicates that premotor inhibition, which is probably reflected by the Nogo-N2, is intensified in PD. The P3 was specifically attenuated and delayed after Nogo stimuli in the incompatible condition for PDs. Assuming that the Nogo-P3 reflects the evaluation of successful motor inhibition, our data show that this process is attenuated and delayed in PD but mainly in the incompatible task. The results suggest that inhibitory deficits in PD are only evident in complex (incompatible) stimulus–response mappings. These effects are probably due to an overstrain of striatal processes.     

Emotion processing in Parkinson's disease: dissociation between early neuronal processing and explicit ratings.

OBJECTIVE: Patients suffering from Parkinson's disease (PD) have a diminished ability to discriminate facial expressions of emotion. We investigated early emotion discrimination deficits in PD by means of event-related potentials (ERPs). METHODS: Emotional pictures were presented to 14 PD patients and 14 healthy controls in a rapid serial visual presentation paradigm (three frames per second) while EEG was recorded. In addition, valence and arousal ratings were obtained for a representative subsample of 54 pictures. RESULTS: PD patients rated pictures of highly arousing content as less exciting than did healthy controls. Pictures of high compared to low emotional arousal were associated with a pronounced relative negative shift in the ERP waveform over parietal and occipital sites developing about 220 ms after picture onset. This early posterior negativity (EPN) did not differ between PD and control group. CONCLUSIONS: This dissociation of affective ratings and early ERP components supports the view that PD is associated with blunted emotional responses, but there is no evidence for a deteriorated early visual processing of emotional stimuli. SIGNIFICANCE: Frequently reported deficits in emotion discrimination are likely not due to deficits in early emotion processing.     

Hemispheric asymmetries and prosodic emotion recognition deficits in Parkinson's disease

While Parkinson's disease (PD) has traditionally been described as a movement disorder, there is growing evidence of cognitive and social deficits associated with the disease. However, few studies have looked at multi-modal social cognitive deficits in patients with PD. We studied lateralization of both prosodic and facial emotion recognition (the ability to recognize emotional valence from either tone of voice or from facial expressions) in PD. The Comprehensive Affect Testing System (CATS) is a well-validated test of human emotion processing that has been used to study emotion recognition in several major clinical populations, but never before in PD. We administered an abbreviated version of CATS (CATS-A) to 24 medicated PD participants and 12 age-matched controls. PD participants were divided into two groups, based on side of symptom onset and unilateral motor symptom severity: left-affected (N = 12) or right-affected PD participants (N = 12). CATS-A is a computer-based button press task with eight subtests relevant to prosodic and facial emotion recognition. Left-affected PD participants with inferred predominant right-hemisphere pathology were expected to have difficulty with prosodic emotion recognition since there is evidence that the processing of prosodic information is right-hemisphere dominant. We found that facial emotion recognition was preserved in the PD group, however, left-affected PD participants had specific impairment in prosodic emotion recognition, especially for sadness. Selective deficits in prosodic emotion recognition suggests that (1) hemispheric effects in emotion recognition may contribute to the impairment of emotional communication in a subset of people with PD and (2) the coordination of neural networks needed to decipher temporally complex social cues may be specifically disrupted in PD.     

Cognitive impairment and dementia in Parkinson's disease

Relatively subtle cognitive disturbances may be present from the initial stages of Parkinson's disease (PD) that progress in many patients to a more severe cognitive impairment and dementia. Several of the initial deficits are ascribed to failure in the frontal-striatal basal ganglia circuits and involve executive defects in planning, initiation, monitoring of goal-directed behaviors and working-memory. Other non-demented PD patients also exhibit visuospatial and memory deficits more representative of posterior cortical functioning and fail performing naming or copying tasks. Major differences in the overall rate of cognitive decline among PD patients support the co-existence of at least two patterns of involution, differentiating a relatively slow decline of fronto-striatal deficits from a more rapid decline of posterior-cortical deficits, with different pathophysiological substrates, genetics, prognosis and response to drugs used to treat the motor symptoms of PD.     

Human immunodeficiency virus dementia: evidence of a subcortical process from studies of fine finger movements

HIV-1 associated dementia is the major manifestation of HIV-1 within the central nervous system and a devastating disease which is characterized by cognitive, motor, and emotional deficits. HIV-1 associated minor motor deficits can manifest as psychomotor slowing and predict the later development of HIV-1 associated dementia, AIDS, and death. These minor motor deficits can be described, e.g., by electrophysiological assessment of basal ganglia motor function (frequency of most rapid alternating finger movements, reaction and contraction times of most rapid index finger extensions). Minor motor deficits quantified by contraction times can be subdivided into a more incipient and a more sustained type of deficit. Parallel examination of motor function and positron emission tomography, magnetic resonance spectroscopy of the basal ganglia, or SPECT helps to point to the basal ganglia as a pivotal point of HIV-1 associated CNS pathology.     

Recognition of emotion from facial,prosodic and written verbal stimuli in Parkinson's disease

Although the basal ganglia are thought to be important in recognizing emotion, there is contradictory evidence as to whether patients with Parkinson's disease (PD) have deficits in recognizing facial expressions. In addition, few studies have examined their ability to recognize emotion from non-visual stimuli, such as voices. We examined the ability of PD patients and age-matched controls to recognize emotion in three different modalities: facial, prosodic, and written verbal stimuli. Compared to controls, PD patients showed deficits in recognizing fear and disgust in facial expressions. These impairments were not seen in their recognition of prosodic or written verbal stimuli. This modality-specific deficit suggests that the neural substrates for recognizing emotion from different modalities are not fully identical.     

Impaired L1 and executive control after left basal ganglia damage in a bilingual Basque-Spanish person with aphasia

Bilinguals must focus their attention to control competing languages. In bilingual aphasia, damage to the fronto-subcortical loop may lead to pathological language switching and mixing and the attrition of the more automatic language (usually L1). We present the case of JZ, a bilingual Basque-Spanish 53-year-old man who, after haematoma in the left basal ganglia, presented with executive deficits and aphasia, characterised by more impaired language processing in Basque, his L1. Assessment with the Bilingual Aphasia Test revealed impaired spontaneous and automatic speech production and speech rate in L1, as well as impaired L2-to-L1 sentence translation. Later observation led to the assessment of verbal and non-verbal executive control, which allowed JZ's impaired performance on language tasks to be related to executive dysfunction. In line with previous research, we report the significant attrition of L1 following damage to the left basal ganglia, reported for the first time in a Basque-Spanish bilingual. Implications for models of declarative and procedural memory are discussed.     

I spy with my little eye: The detection of changes in emotional faces and the influence of facial feedback in Parkinson disease

Background and purpose

Parkinson disease (PD) is a progressive neurodegenerative disorder that affects the motor system but also involves deficits in emotional processing such as facial emotion recognition. In healthy participants, it has been shown that facial mimicry, the automatic imitation of perceived facial expressions, facilitates the interpretation of the emotional states of our counterpart. In PD patients, recent studies revealed reduced facial mimicry and consequently reduced facial feedback, suggesting that this reduction might contribute to the prominent emotion recognition deficits found in PD.

Methods

We investigated the influence of facial mimicry on facial emotion recognition. Twenty PD patients and 20 healthy controls (HCs) underwent a classical facial mimicry manipulation (holding a pen with the lips, teeth, or nondominant hand) while performing an emotional change detection task with faces.

Results

As expected, emotion recognition was significantly influenced by facial mimicry manipulation in HCs, further supporting the hypothesis of facial feedback and the related theory of embodied simulation. Importantly, patients with PD, generally and independent from the facial mimicry manipulation, were impaired in their ability to detected emotion changes. Our data further show that PD patients' facial emotional recognition abilities are completely unaffected by mimicry manipulation, suggesting that PD patients cannot profit from an artificial modulation of the already impaired facial feedback.

Conclusions

These findings suggest that it is not the hypomimia and the absence of facial feedback per se, but a disruption of the facial feedback loop, that leads to the prominent emotion recognition deficit in PD patients.     

High-frequency rTMS improves time perception in Parkinson disease

Patients with Parkinson disease (PD) are impaired in time processing. The authors investigated the effects of high-frequency (5 Hz) repetitive transcranial magnetic stimulation (rTMS) in patients with PD performing a time reproduction task. The authors found significant improvement in time processing induced by rTMS when trains were applied over the right dorsolateral prefrontal cortex (DLPFC) but not over the supplementary motor area, suggesting that the circuit involving the basal ganglia and the DLPFC might constitute the neural network subserving time perception.     

Impaired L1 and executive control after left basal ganglia damage in a bilingual Basque–Spanish person with aphasia

Bilinguals must focus their attention to control competing languages. In bilingual aphasia, damage to the fronto-subcortical loop may lead to pathological language switching and mixing and the attrition of the more automatic language (usually L1). We present the case of JZ, a bilingual Basque–Spanish 53-year-old man who, after haematoma in the left basal ganglia, presented with executive deficits and aphasia, characterised by more impaired language processing in Basque, his L1. Assessment with the Bilingual Aphasia Test revealed impaired spontaneous and automatic speech production and speech rate in L1, as well as impaired L2-to-L1 sentence translation. Later observation led to the assessment of verbal and non-verbal executive control, which allowed JZ's impaired performance on language tasks to be related to executive dysfunction. In line with previous research, we report the significant attrition of L1 following damage to the left basal ganglia, reported for the first time in a Basque–Spanish bilingual. Implications for models of declarative and procedural memory are discussed.