Hemispheric specialization of the basal ganglia during vocal emotion decoding: Evidence from asymmetric Parkinson's disease and 18FDG PET

Abstract

The possible hemispheric specialization of the basal ganglia during emotional prosody (i.e., vocal emotion) processing has still to be elucidated. Coupled with affective measures and neuroimaging, Parkinson's disease offers a unique opportunity to study this question, on account of its characteristically asymmetric striatal dysfunction, which translates into predominantly contralateral motor symptoms. We investigated the cerebral metabolic bases of emotional prosody recognition in patients with Parkinson's disease with left- versus right-lateralized motor symptoms, postulating that patients with greater right hemispheric brain dysfunction have a specific impairment that correlates with the metabolic modification of a brain network known to be involved in emotional prosody. A total of 38 patients performed a validated emotional prosody recognition task and underwent a resting-state F-18 fluorodeoxyglucose PET scan, as well as clinical, motor, neuropsychological, and psychiatric assessments. Patients' performances were compared with those of 45 healthy controls. As expected, vocal emotion recognition was significantly poorer among patients with left-sided motor symptoms than among both right-sided patients and controls. There was no significant difference between right-sided patients and controls. This effect was observed for both the total score and the happiness subscore. Interestingly, regressions showed that the greater the emotional misattribution, the greater the patients' age and asymmetric motor symptom severity. Finally, at the metabolic level, positive correlations were found between the happiness recognition subscore and the metabolism of the right orbitofrontal cortex in patients with left-sided motor symptoms. A right orbitofrontal-basal ganglia coupling seems to be specifically involved in the vocal emotion recognition deficit observed in Parkinson's disease. The asymmetry of motor symptoms is thus an important clinical factor, in that it may influence the presence or severity of affective disorders in Parkinson's disease.

Early‐Stage Parkinson's Patients Show Selective Impairment in Reactive But Not Proactive Inhibition

“…These studies, however, are based on clinical scales and questioners, and this might limit the generalizability of their results. The most consistent performance‐based evidence suggest that RPD patients tend to have a specific impairment in some language domains, whereas LPD patients show visuospatial impairments and impaired vocal emotion processing . All of these functions have clear lateralization in healthy subjects, suggesting that lateralized PD patients represent a good model to assess whether inhibitory control relies on a right‐lateralized network .…”

“…The most consistent performancebased evidence suggest that RPD patients tend to have a specific impairment in some language domains, 36 whereas LPD patients show visuospatial impairments 41,42 and impaired vocal emotion processing. 43,44 All of these functions have clear lateralization in healthy subjects, suggesting that lateralized PD patients represent a good model to assess whether inhibitory control relies on a right-lateralized network. 17 We hypothesized that, if this was the case, than LPD patients should be more impaired than RPD patients in both proactive and reactive inhibition.…”

Social perceptual function in parkinson’s disease: A meta-analysis

“…Pell & Leonard, 2003;, words (e.g. Brück et al, 2011, Péron et al, 2010Stirnimann et al, 2018), pseudo-sentences, and semantic sentences (e.g. Ariatti et al, 2008;Lima et al, 2013;Paulmann & Pell, 2010).…”

“…This was an important question to address, because for PwPD, the onset of motor symptoms is typically unilateral. This asymmetry is associated with more pronounced dopaminergic denervation in the basal ganglia, contralateral to the presenting symptoms (De Risi et al, 2018;Stirnimann et al, 2018), with this pattern said to persist even after motor symptom presentation becomes bilateral (Garrido-Vásquez et al, 2012;Ille et al, 2016). As there is some evidence for right hemispheric specialisation for emotional and social processing (e.g.…”

The basal ganglia and the cerebellum in human emotion

“…, 2010 ). Interestingly, the impact of STN DBS on emotion or mood may depend upon the laterality of the substantia nigra degeneration in Parkinson’s disease: patients with predominantly left-sided motor impairments (right BG dysfunction) showed worse vocal emotion recognition for happy stimuli than patients with right-sided impairments (left BG dysfunction) or controls ( Stirnimann et al. , 2018 ).…”