Abstract

Background: Survival may depend on the ability to efficiently identify threats signaled by the emotional content of facial expressions. While current neural models of facial emotion processing do not prominently feature the basal ganglia, evidence from clinical and functional imagi¬ng studies suggest involvement of the ventral striatum. Methods: To assess the specific role of the basal ganglia in emotion processing, we compared basic facial emotion identification in 23 young patients with a pure focal basal ganglia stroke (mean age 44.9 ± 11.6; 10 males) to 68 matched healthy controls (43.8 years ± 14.0; 27 males). We used quantitative MRI lesion analysis to assess the relationship between basal ganglia location and basic emotion identification. To assess whether facial emotion identification might be related to non-specific lesion effects, we also assessed a wide range of cognitive and motor abilities and screened participants for co-morbid conditions such as depression or anxiety. In addition, we assessed social behavior in terms of social adaptability and the ability to return to work. Results: (1) Basic emotion identification was impaired following focal lesions limited to the basal ganglia. (2) The identification impairment was limited to threat-related emotions, including anger, fear and disgust identification, suggesting a role for the basal ganglia in threat detection. These findings may reflect altered gating mechanisms for facial emotion displays conveying threat signals, with the basal ganglia selecting information relevant to safety. (3) We found that emotion identification impairments adversely affect social behavior, suggesting that emotion identification skills may be of substantial practical importance, and should be considered in the clinical assessment and rehabilitation of patients with basal ganglia lesions. Conclusions: Dorsolateral striatal lesions may affect threat-related emotion identification by disrupting limbic basal ganglia-thalamocortical loop functions associating threat detection with selection of appropriate escape or defensive actions that can preserve individual safety. From a clinical perspective, while the impact of emotion identification impairment on social behavior should be more thoroughly examined in further studies, the consequences of basal ganglia damage appear to be detectible at the individual level. Figure legend: Lesion overlap for patients with identification impairments for anger (red); fear (blue) disgust (green) and all threat emotion (yellow).

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