Subcortical involvement in body and mental action verb processing: an electrophysiological registration study
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1
Ghent University, Belgium
Electrophysiological registration of semantic processing generally involves paradigms eliciting semantic violations on recognition memory or semantic judgement tasks. The N400, LAN (left anterior negativity) and P600 may be sensitive to semantic judgement alterations on cortical level (Olichney et al., 2008). The LAN is a negative-going peak around 400 ms after word presentation and is typically elicited by morpho-syntactic violations (Coulson 1998). In the context of semantic processing, P600 components have been observed in response to thematic and other semantic violations (Kuperberg 2003; Kim 2005).
Although semantic effects of subcortical modulation have been well described, it is unclear if semantic related local field potentials can be elicited in the main subcortical nuclei. Direct registration of language elicited EEG in the deep brain nuclei is only possible in patients recruited for deep brain stimulation as a treatment for their illness and in the short period after the operation that the electrode leads are still externalized. The current research project focusses on the electrophysiological registration of semantics (body versus mental action verbs) within the thalamus, subthalamic nucleus (STN) and the pedunculopontine nucleus (PPN) within 1 week after DBS-implantation.
Methods
Patients
The current study included 18 patients with deep brain electrodes within the STN (mean age 59 (45-71); 8 male/10 female), 2 patients with electrodes in the thalamus (mean age 64 (56-73)/1 male/1 female) and 1 male patient with PPN stimulation (age 50). The difference in number of patients corresponds with the prevalence of indications for DBS in the course of two years in our centre. All patients were right-handed and testing was performed with and without medication.
Paradigms
The event-related potential (ERP)-paradigms consisted of 30 body action verbs (e.g. to sew, to point) and 30 mental action verbs without manual action connotation (e.g. to leave, to develop). All verbs consisted of two syllables, matched with respect to word form frequency, and imageability (Duyck 2004). The body action and mental action verbs were shown consecutively in a randomized order, with a stimulus duration of 1s and without interstimulus interval.
Materials
An in-house made interface between the registration device (Neurosoft) and the STN/thalamus/PPN leads was connected to the bilateral (temporarily) externalized DBS-contacts. The leads are numbered from 0 to 3, with 0 as the most distal and 3 as the most proximal contact. Data was collected using a 32-channel SynAmp (Neuroscan) amplifier. EEG analysis (ERP analysis and source localizing) was performed in all nuclei using BrainVision Analyzer 2 (Brain Products, Munich, Germany). ERP data were analysed using linear mixed models. All statistical analyses were performed using IBM SPSS Statistics 23.
Results
Within the left STN a source waveform for both body and mental action verbs is demonstrated in a time frame between 150 and 200ms post-stimulus at L0-L1/L1-L2 and L1-L2/L2-L3 (Fig. 1). Significantly higher amplitudes were elicited by body action verbs compared to mental action verbs. In the body action verbs a significant increase of the negative peak amplitude and a decrease of peak latency can be seen after dopaminergic administration, while no changes can be observed in peak amplitude and latency detection in mental action verbs.
Within the PPN, bipolar analysis points to a clear source waveform in the right hemisphere in the OFF condition for making the ‘difference between body and action verbs’. This source waveform can be seen between R0-R1 and R1-R2 in a time frame between 250ms and 450ms (Fig. 2).
Within the thalamus a negative peak and clear lateralization effect in the left hemisphere (L1-L2/L2-L3) can be found with both stimuli (body and mental action verbs) and in a time window between 200-800ms (Fig. 3). In making the ‘difference between both body and mental action verbs’ a positive peak can be demonstrated between 200-500ms.
Discussion
This study reports on the involvement of the STN, PPN and thalamus in semantic processing. Direct registration of EEG activity within these three nuclei allows to bring the temporal characteristics of semantic processing into focus. The results indicate that the three grey deep brain nuclei are involved in semantic processing in a different way. Where the thalamus suggests a significant left lateralized activity between 200-500ms during ‘making the difference between body and mental action verbs’, the PPN seems to be activated for the same time window and demands in the right hemisphere. The lateralization difference suggests an involvement of the PPN in the decision aspect (which is a well-known function of the PPN) in making a semantic differentiation than in semantic processing itself (Gut 2016). The time window occurs prior to the cortical semantic processing (300-600ms). The STN demonstrates a source waveform for both body and mental action verbs in a time frame between 150 and 200ms, which suggests a language modality aspecific (‘tool use’ in this semantic tasks) involvement of the STN in semantic processing. The language modality specific and aspecific demands are both under the influence of dopamine. The current results and methodology encourages new research on the involvement of subcortical grey and white matter in language specific and aspecific language modalities.
Resume in Dutch:
De doelstelling van het overkoepelende project is het opstellen en/of modificeren van modellen van perceptie en taalbegrip, waarin de activiteit van de diepe hersenkernen wordt betrokken. Deze modellen kunnen dan aangewend worden om stoornissen bij verschillende patiëntengroepen beter te begrijpen. Direct onderzoek van de diepe hersenkernen is enkel mogelijk bij patiënten die diepe hersenstimulatie hebben ondergaan, de onderzoeksgroep is op dit vlak een pionier. Deze specifieke studie onderzocht de rol van diepe hersenkernen in de semantische verwerking van verschillende werkwoordtypes.
Resumé en Français :
L'objectif de cette recherche est de créer ou de modifier des modèles de perception et de compréhension de la langue à partir de l’enregistrement de l'activité des noyaux cérébraux profonds chez des humains. Le but ultime étant d’utiliser ces modèles pour mieux comprendre les troubles de langage observés dans différents groupes de patients. L'examen direct des noyaux cérébraux profonds (le thalamus, le noyau sous-thalamique et le noyau pedonculopontin) n’a été possible qu’avec l’aide de patients qui étaient traités par une stimulation cérébrale profonde.
References
Coulson S, King JW, Kutas M. Expect the unexpected: Event-related brain response to morphosyntactic violations. Lang Cogn Process. 1998; 13: 21–58.
Duyck W, Desmet T, Verbeke LP, Brysbaert M. WordGen: a tool for word selection and nonword generation in Dutch, English, German, and French. Behav Res Methods Instrum Comput. 2004 Aug;36(3):488-99.
Gut NK, Winn P. The pedunculopontine tegmental nucleus-A functional hypothesis from the comparative literature. Mov Disord. 2016 May;31(5):615-24. doi: 10.1002/mds.26556. Epub 2016 Feb 16. Review.
Kim, A., & Osterhout, L. (2005). The independence of combinatory semantic processing: Evidence from event-related potentials. Journal of Memory and Language, 52, 205–225.
Kuperberg GR, Sitnikova T, Caplan D, Holcomb PJ (2003) Electrophysiological distinctions in processing conceptual relationships within simple sentences. Brain Res Cogn Brain Res 17: 117–129
Olichney JM, Taylor JR, Gatherwright J, Salmon DP, Bressler AJ, Kutas M, Iragui-Madoz VJ. Patients with MCI and N400 or P600 abnormalities are at very high risk for conversion to dementia. Neurology. 2008 May 6;70(19 Pt 2):1763-70. Epub 2007 Dec 12.
Keywords:
EEG,
Deep Brain Stimulation,
Language,
semantics,
Subthalamic Nucleus,
Thalamus,
pedunculopontine nucleus,
event-related potential (ERP),
Dopamine Agonists,
Parkinson Disease
Conference:
6th Belgian Brain Congress, MONS, Belgium, 8 Oct - 8 Oct, 2016.
Presentation Type:
Poster Presentation
Topic:
Brain and brain diseases: between heredity and environment
Citation:
Bruggeman
A,
De Keyser
K,
Aerts
A,
Van Mierlo
P,
Boon
P,
Buysse
H,
Raedt
R,
Van Roost
D,
Santens
P and
De Letter
M
(2016). Subcortical involvement in body and mental action verb processing: an electrophysiological registration study.
Conference Abstract:
6th Belgian Brain Congress.
doi: 10.3389/conf.fnagi.2016.03.00047
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Received:
30 Jun 2016;
Published Online:
06 Jul 2016.
*
Correspondence:
MD. Arnout Bruggeman, Ghent University, Ghent, Oost-Vlaanderen, 9000, Belgium, arnout.bruggeman@ugent.be