No effect of subthalamic deep brain stimulation on metacognition in Parkinson's disease

Abstract

Deep brain stimulation of the subthalamic nucleus (STN-DBS) is a powerful treatment in Parkinson's disease (PD), which provides a positive effect on motor symptoms although the way it operates on high cognitive processes such as metacognition remains unclear. To address this issue, we recorded electroencephalogram (EEG) of PD patients treated with STN-DBS that performed a reversal learning (RL) paradigm endowed with metacognitive self-assessment. We considered two stimulation conditions, namely DBS-ON (stimulation on) and DBS-OFF (stimulation off), and focused our EEG-analysis on the frontal brain region due to its involvement on high cognitive processes. We found a trend towards a significant difference in RL ability between stimulation conditions. STN-DBS showed no effect on metacognition, although a significant association between accuracy and decision confidence level held for DBS OFF, but not in the case of DBS ON. In summary, our study revealed no significant effect of STN-DBS on RL or metacognition.

Figure 1

Reversal Learning (RL) Paradigm and EEG Clusters. (A) The RL task consisted of trials with and without metacognitive assessment, which we termed as Metacognitive and Standard trials, respectively. The order of trial presentation was randomized. (B) Two EEG clusters consisting of channels (FP1, FP2, F3, Fz, F4, Fc1, Fc2) and (F3, Fz, F4) were considered for further analysis.

Figure 2

Effect of DBS on reversal Learning (RL) and performance parameters. The violin- type graphs depict the distribution, mean and median of each variable for both stimulation conditions (DBS-OFF and DBS-ON). (A) number of trials to reach reversal (TR); (B) number of consecutive errors after reversal (CEAR); (C) number of random switch (RS) (trials were patients switched symbols after getting positive feedback); (D) strategy change after probabilistic error (SCAPE) (trials after probabilistic error were patients switched symbols directly); (E) response time (RT) and (F) accuracy.

Figure 3

Analysis of relative type 2 sensitivity: meta-d (observed type 2 sensitivity) and d (type 1 sensitivity) for each subject across conditions (DBS-OFF and DBS-ON). We computed such parameters by using the methodology provided by Maniscalco and Lau (2012). Note that if meta-d = d, then a subject is “ideal” from a metacognitive perspective, while the degree to which meta-d is smaller than d reflects the degree to which the subject is inefficient in metacognitive terms.

Figure 4

Electrophysiological results. The graphs depict mean power across patients by comparing power of trials corresponding to (A) DBS-OFF and DBS-ON regardless of the confidence level to identify a marker of stimulation, (B) low and high confidence level regardless of stimulation condition to identify a marker of confidence; (C) low and high confidence level under no effect of stimulation and (D) DBS-ON and DBS-OFF by considering a high level of confidence. For the calculation of power, we considered a 7-EEG channel frontal cluster.