Topography of emotional valence and arousal within the motor part of the subthalamic nucleus in Parkinson’s disease

Clinical motor and non-motor effects of deep brain stimulation (DBS) of the subthalamic nucleus (STN) in Parkinson's disease (PD) seem to depend on the stimulation site within the STN. We analysed the effects of the position of the stimulation electrode within the motor STN on subjective emotional experience, expressed as emotional valence and arousal ratings to pictures representing primary rewards and aversive fearful stimuli in 20 PD patients. Patients’ ratings from both aversive and erotic stimuli matched the mean ratings from a group of 20 control subjects at similar position within the STN. Patients with electrodes located more posteriorly reported both valence and arousal ratings from both the rewarding and aversive pictures as more extreme. Moreover, posterior electrode positions were associated with a higher occurrence of depression at a long-term follow-up. This brain–behavior relationship suggests a complex emotion topography in the motor part of the STN. Both valence and arousal representations overlapped and were uniformly arranged anterior-posteriorly in a gradient-like manner, suggesting a specific spatial organization needed for the coding of the motivational salience of the stimuli. This finding is relevant for our understanding of neuropsychiatric side effects in STN DBS and potentially for optimal electrode placement.

Appendix A Table A1.
The gradients of emotional ratings in respect to the antero-posterior position of the left and right active electrode contacts. Left    Gradients in affective ratings are expressed in terms of a change of rating per 1mm (when significant), the gradient significance (χ 2 statistics and P-value of the model-submodel test), and the equality point, defined as the position along the antero-posterior axis in which patients, on average, rated the stimuli equally to control subjects. No gradient differed between DBS conditions. The gradients of emotional ratings in respect to the antero-posterior position of the active contact on the right electrode.
The legend is the same as for Fig. A1.

Appendix B
Can the position-related emotional effects be explained by micro-lesion?
As the DBS electrode insertion causes micro-lesion of the STN, we asked whether the observed variability on the topographic gradients in the emotional ratings could not be explained by the micro-lesions in the STN rather than the position of the active DBS electrode contact.
We quantified STN micro-lesions in terms of the volume of STN motor, associative, and limbic territories impacted by the DBS electrode. The lesioned volume of each territory on In conclusion, the emotional gradients in the antero-posterior directions (as described in Results) could simply not be attributed to the effects of the DBS-induced micro-lesion.
Can the variability in affective ratings be explained by the pure presence of the DBS electrode?
In the Results section, we described how the valence and arousal ratings gradually changed with the position of the active contact of DBS electrodes. Surprisingly, we did not find a difference in the strength of these gradients between the DBS ON and OFF conditions, which insinuated that chronic rather than acute effects could be associated with the ratings changes. We thus further asked about the nature of these gradients. Could the gradual rating changes be best explained by the position of the active contacts, or rather by the position of the DBS electrode per se?
To answer this question, we built alternative models of valence and arousal ratings in terms of the position of the tip of the DBS electrodes (instead of the position of the active electrode contact). We speculated that if the gradual changes in the ratings were associated with the presence of the DBS electrode regardless of which electrode contact was active, we would have observed much stronger gradients in terms of the electrode tip. If, on the other hand, the gradual emotional changes were implied by DBS delivered through the active contact, a stronger gradient would have been observed considering the active electrode contacts.
The original and the alternative gradients are given in Table B1, where the strength of each gradient and the quality of the corresponding model fit are compared. It is evident that both the strength of the gradient (i.e. the change in rating associated with 1 mm change in the electrode position) and the fit quality were higher for models that explained the ratings in terms of the active electrode contact. We thus concluded that the changes in the emotional experience were caused by the DBS delivered through the active contact rather than by the pure presence of the DBS electrode within the STN. Gradients in affective ratings are expressed in terms of a change in rating per 1 mm, the gradient significance (the P-value of the model-submodel test), and the Akaike information criterion (AIC) expressing the quality of the model fit (better fits lead to smaller AIC values).