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. 2022 Jun 1:13:875950.
doi: 10.3389/fneur.2022.875950. eCollection 2022.

Emotional Word Processing in Patients With Juvenile Myoclonic Epilepsy

Lucas Johannes Rainer  1   2   3 , Martin Kronbichler  2   4 , Giorgi Kuchukhidze  1 , Eugen Trinka  1   2   5   6 , Patrick Benjamin Langthaler  1   7 , Lisa Kronbichler  2   3 , Sarah Said-Yuerekli  1   4 , Margarita Kirschner  1 , Georg Zimmermann  8   9 , Julia Höfler  1 , Elisabeth Schmid  1 , Mario Braun  4
Affiliations

Emotional Word Processing in Patients With Juvenile Myoclonic Epilepsy

Lucas Johannes Rainer et al. Front Neurol. .

Abstract

Objective: According to Panksepp's hierarchical emotion model, emotion processing relies on three functionally and neuroanatomically distinct levels. These levels comprise subcortical networks (primary level), the limbic system (secondary level), and the neocortex (tertiary level) and are suggested to serve differential emotional processing. We aimed to validate and extend previous evidence of discrete and dimensional emotion processing in patient with juvenile myoclonic epilepsy (JME).

Methods: We recorded brain activity of patients with JME and healthy controls in response to lexical decisions to words reflecting the discrete emotion fear and the affective dimension negativity previously suggested to rely on different brain regions and to reflect different levels of processing. In all study participants, we tested verbal cognitive functions, as well as the relationship of psychiatric conditions, seizure types and duration of epilepsy and emotional word processing.

Results: In support of the hierarchical emotion model, we found an interaction of discrete emotion and affective dimensional processing in the right amygdala likely to reflect secondary level processing. Brain activity related to affective dimensional processing was found in the right inferior frontal gyrus and is suggested to reflect tertiary level processing. Psychiatric conditions, type of seizure nor mono- vs. polytherapy and duration of epilepsy within patients did not have any effect on the processing of emotional words. In addition, no differences in brain activity or response times between patients and controls were observed, despite neuropsychological testing revealed slightly decreased verbal intelligence, verbal fluency and reading speed in patients with JME.

Significance: These results were interpreted to be in line with the hierarchical emotion model and to highlight the amygdala's role in processing biologically relevant stimuli, as well as to suggest a semantic foundation of affective dimensional processing in prefrontal cortex. A lack of differences in brain activity of patients with JME and healthy controls in response to the emotional content of words could point to unaffected implicit emotion processing in patients with JME.

Keywords: dimensional emotion; discrete emotion; implicit emotion processing; juvenile myoclonic epilepsy (JME); neuropsychology.

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Conflict of interest statement

ET reports personal fees from EVER Pharma, Marinus, Argenix, Arvelle/Angelini, Medtronic, Bial – Portela, S.A., NewBridge, GL Pharma, GlaxoSmithKline, Hikma, Boehringer Ingelheim, LivaNova, Eisai, UCB, Biogen, Genzyme Sanofi, GW Pharmaceuticals, and Actavis outside the submitted work; his institution received grants from Biogen, UCB Pharma, Eisai, Red Bull, Merck, Bayer, the European Union, FWF Osterreichischer Fond zur Wissenschaftsforderung, Bundesministerium fr Wissenschaft und Forschung, and Jubilaumsfond der sterreichischen Nationalbank outside the submitted work. GZ gratefully acknowledges the support of the WISS 2025 project; IDA-Lab Salzburg (20204-WISS/225/197-2019 and 20102-F1901166-KZP). The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Activation clusters revealed by the whole brain analyses. Regions that elicited increased activation for words compared to baseline (irrespective of group) are shown in yellow. All clusters were extracted at a threshold of p < 0.001 [uncorrected, with a FWE cluster-level-correction (p < 0.05)].
Figure 2
Figure 2
fMRI results for our conditions in the right amygdala (top left), right inferior frontal cortex (top right), and left inferior frontal gyrus (bottom left). Errror bars indicate standard error.
See this image and copyright information in PMC

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