The effect of frontoparietal paired associative stimulation on decision-making and working memory

Abstract

Previous single-site neurostimulation experiments have unsuccessfully attempted to shift decision-making away from habitual control, a fast, inflexible cognitive strategy, towards goal-directed control, a flexible, though computationally expensive strategy. We employed a dual-target neurostimulation approach in 30 healthy participants, using cortico-cortical paired associative stimulation (ccPAS) to target two key nodes: lateral prefrontal cortex (LPFC) and intraparietal sulcus (IPS), to test whether decision-making can be artificially shifted from habitual toward goal-directed control. Participants received three active stimulations, delivered at least six days apart (each involving 100 paired pulses over the IPS and LPFC, varying the interstimulus interval): two interventional, time-relevant ccPAS (10 msec interval) and one control, non-time-relevant ccPAS (100 msec interval). Following stimulation, participants completed a sequential learning task, measuring goal-directed/habitual control, and a working memory task. IPS→LPFC ccPAS (stimulating IPS, then LPFC with a 10 msec interval) shifted decision-making from habitual toward goal-directed control, compared to control ccPAS. There was no effect of LPFC→IPS ccPAS, nor an effect of any PAS condition on working memory. Previous studies have shown ccPAS effects outside the motor domain targeting prefrontal regions on response inhibition, attentional bias, and alpha asymmetry. The present study measures the behavioural effects of parietal-prefrontal PAS, focusing on a highly complex decision-making task and working memory. If confirmed in larger studies, this would be the first instance of neurostimulation successfully shifting decision-making from habitual to goal-directed control, putatively via inducing long-term potentiation between the IPS and LPFC. However, we found no effect in the other direction (LPFC→IPS ccPAS), and no effect on working memory overall. PAS is a relatively new neuromodulatory technique in the cognitive arsenal, and this study could help guide future approaches in healthy and disordered decision-making.

Keywords: Decision-making; Goal-directed; Habitual; Paired associative stimulation; Psychiatry.

Fig. 1

Neurostimulation montage and task design. A. Cortico-cortical paired associative stimulation (ccPAS) consisted of one coil positioned over the right intraparietal sulcus (IPS) (20° tilt posteriorly) and one coil positioned over the right lateral prefrontal cortex (LPFC) (20° tilt anteriorly), under neuronavigation (see insert). B. Illustration of target regions [x,y,z, in Montreal Neuroimaging Index (MNI) coordinates (in mm)]: the right LPFC (blue: 50,16,26), and right inferior parietal sulcus (yellow: 30,–60,50). For visualisation purposes only, we depict an example of the white matter tracts connecting IPS and LPFC coordinates. This illustration was made using previously-published diffusion-weighted imaging data from the Human Connectome Project (healthy subject dataset), employing deterministic tractography on a standardized structural connectome [see previous publication for methodological details and full results (Horn et al., 2017)]. C. The two-step task involved a first level of selection between two symbols, with each having a fixed probability of leading to a subsequent set of stimuli. At the second level, participants selected one of the new symbols, which were each associated with a differential probability of monetary reward. The second-level contingencies (i.e., reward probabilities) shifted slowly and independently over time according to Gaussian random walks; one example is illustrated in Fig. 1C). D. The working memory task began with a fixation cross (500 msec) before presenting either three or six lines rotated around the fixation cross (3 lines in 75 trials; 6 lines in 75 trials; randomised order across trials), also for 500 msec. Last, participants had to rotate a probe line using the mouse, attempting to match its orientation to the line displayed in that location on the previous screen (unlimited time allowed).

Fig. 2

Two-step task performance under ccPAS conditions. The weighting of goal-directed (model-based: closer to w = 1) to habitual control (model-free: closer to w = 0) following control stimulation (grey points), lateral prefrontal cortex (LPFC) → intraparietal sulcus (IPS) 10 msec interval ccPAS (pink points), and following IPS→LPFC 10 msec interval ccPAS (teal points). In the IPS→LPFC condition, participants significantly shifted toward model-based (goal-directed) and away from model-free (habitual) control of behaviour, compared to the control condition (non-parametric test, p = .028). Red line = median; blue dotted line = mean; purple patch = standard error of the mean; * = p < .05.

Fig. 3

Working memory performance under ccPAS conditions. Effect of ccPAS on precision of responses (inverse of the SD), our key measure on the visual working memory task, under control stimulation (grey points), lateral prefrontal cortex (LPFC) → intraparietal sulcus (IPS) stimulation (pink points), and following IPS→LPFC stimulation (teal points). There was no main effect of ccPAS condition on working memory (p = .369). Red line = median; blue dotted line = mean; purple patch = standard error of the mean.