Impulse control disorders (ICDs) as classified in the Diagnostic and Statistical Manual of Mental Disorders, 5th Edition (DSM-5, American Psychiatric Association, 2013) are conditions involving problems of emotional and behavioral self-control, including intermittent explosive disorder (IED), kleptomania, pyromania, and other specified or unspecified ICDs. More commonly observed in PD are diminished control over gambling, sexual behaviors, eating, shopping, hobbyism, non-goal directed actions (punding) and medication use (Dopamine Dysregulation Syndrome, DDS) (Weintraub et al., 2009). The Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease Rating Scale (QUIP-RS) is the most widely used and well-validated scale for measuring likelihood and severity of ICDs in PD (Weintraub et al., 2012). As the name suggests, this scale intends to measure severity of both impulsive and compulsive disorders. Its questions therefore relate to impulsive as well as compulsive aspects of problematic behaviors, i.e., excessive urges, distressing desires, and obsessive thinking. The total score, however, is defined as severity of ICD without sub-scores for impulsive or compulsive aspects.

Complicating efforts to disambiguate impulsivity and compulsivity in commonly used scales, there has not always been consensus about the definition of impulsivity itself. Many authors agree upon a definition of impulsivity as a tendency to act prematurely with little foresight, a failure to suppress inappropriate motor, cognitive or emotional responses. This definition implies that impulsivity is a multifaceted construct requiring assessment with multiple distinct paradigms. The most widely used paradigms assess impulsivity as: (1) impaired negative feedback learning, e.g., the Iowa Gambling Task (Bechara et al., 1997) or the Probabilistic Selection Task (Frank et al., 2007); (2) a preference for small immediate reward over larger delayed reward, i.e., delayed discounting tasks (Loewenstein, 1988); (3) making responses that are premature or should be withheld, e.g., the Go/No Go Task (Ballanger et al., 2009) or Stroop test (Stroop, 1935).

The most common disorders of compulsivity are defined in the DSM-5 under Obsessive-Compulsive and Related Disorders (OCRD). These include obsessive-compulsive disorder (OCD), body dysmorphic disorder, hoarding disorder, trichotillomania (hair pulling disorder) and excoriation (skin-picking) disorder. The DSM-5 also allows for the identification of compulsions in other mental disorders, defining compulsions as repetitive behaviors or mental acts, such as hand washing, ordering, checking, praying, counting, or repeating words, which the individual feels driven to perform in response to an obsession or according to rules that must be applied rigidly. Compulsions are usually aimed at preventing or reducing anxiety, distress, or dreaded events, despite insight that the behaviors are not realistically connected to these outcomes. Severity of the prototypical disorder of compulsivity, OCD, can be measured with clinician-rated scales such the Maudsley Obsessive-Compulsive Inventory (MOCI, Hodgson and Rachman, 1977), or the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS, Goodman et al., 1989). Examples of transdiagnostic compulsivity questionnaires are the DSM-5 obsessive–compulsive spectrum scale (LeBeau et al., 2013) and the Padua Inventory (Sternberger and Burns, 1990).

As a cognitive construct, compulsivity, like impulsivity, may be decomposed into various factors of a mainly cognitive, affective or motivational nature (Figee et al., 2016). First, similar to impulsivity, compulsivity implies engagement in self-defeating repetitive behaviors, which may be related to altered reward or punishment sensitivity. Second, the diminished ability to ignore or stop unwanted ideas or actions suggests the presence of cognitive or behavioral inflexibility, as measured with reversal-learning tasks (i.e., Wisconsin Card Sorting Task, Grant and Berg, 1948) or attentional set-shifting tasks (i.e., Trail Making Task, Ardouin et al., 1999). Third, habitual responding and diminished goal-directed activity suggests excessive habit-learning, as measured with instrumental or model-based learning paradigms (Daw et al., 2005). However, firm consensus about the definition of compulsivity as a cognitive construct remains to be established. Further, paradigms which explicitly test compulsivity are difficult to develop because compulsive behaviors are often triggered by person-specific circumstances that are challenging to recreate in generalizable tasks. In addition, there may be overlap between impulsivity and compulsivity particularly in reinforcement learning paradigms. Nevertheless, paradigms testing cognitive and behavioral flexibility and habit-learning tap into important aspects of compulsivity which we use in the present review.

We conducted a literature search using the Pubmed database for articles published between January 1st 2002 and June 27th 2019. Keywords for impulsivity associated with subthalamic DBS in PD were based on ICDs, associated scales, and neurocognitive paradigms:

Subthalamic DBS, Parkinson, Impulsivity, Impulse control disorder, Intermittent Explosive Disorder, Kleptomania, pyromania, gambling, sexual behaviors, eating, shopping, hobbyism, punding, Dopamine Dysregulation syndrome, QUIP-RS, extinction learning, reward choice, response inhibition, Barratt Impulsiveness Scale, The Iowa Gambling Task, Instrumental Learning Task, The Game of Dice Task, The Temporal Discounting Task, Deal or No Deal, Cambridge Gambling Task, The Probabilistic selection task, Status Quo Task, Auditory two-alternative forced choice task, The Go/No-Go task, The Stroop Test.

Similarly, for compulsivity we used the following keywords:

Subthalamic DBS, Parkinson, compulsivity, Obsessive-Compulsive Disorder (OCD), OCRD, body dysmorphic disorder, hoarding, trichotillomania, excoriation, hand washing, ordering, checking, praying, counting or repeating words, Maudsley Obsessive-Compulsive Inventory, Yale-Brown Obsessive-Compulsive Scale, Obsessive–Compulsive Spectrum Scale, Padua Inventory, reward punishment sensitivity, cognitive inflexibility, habit learning, probabilistic reversal-learning, attentional set-shifting tasks, habit-learning, devaluation, Trail Making Task, Wisconsin Card Sorting Task, Probabilistic classification task.

After the initial search, a reference analysis was conducted to find additional reports. We excluded studies published before 1999, reviews, animal studies, and computational modeling studies. Only studies investigating the effects of bilateral STN DBS in PD patients were included. Clearly defined assessment tools and dopaminergic medication status at time of testing had to be described. Reports in languages other than English, or that did not include statistical tests, were excluded.

We searched for studies reporting ICDs related to STN-DBS in PD, and for studies measuring DBS-related impulsivity with the following scales or paradigms:

Barratt Impulsiveness Scale (BIS-11, Patton and Stanford, 1995): a 30-item questionnaire designed to assess impulsive personality traits, with sub-scores for attentional impulsivity, motor impulsivity and non-planning impulsivity.

Negative Feedback Learning (Table 1): Iowa Gambling Task (IGT, Bechara et al., 1997), Game of Dice Task (GDT, Brand et al., 2005), Instrumental Learning Task (ILT, Seymour et al., 2016), and Probabilistic Selection Task (Frank et al., 2004, 2007). These paradigms may be used for measuring impulsivity defined as impaired learning from negative feedback. In the IGT and GDT, participants have to balance their choices between safe and advantageous options (card decks or dice rolls with low reward and small losses) and risky and disadvantageous options (high rewards and high losses). In the ILT, participants choose from four abstract pictures based on feedback from previous trials where their choice was either rewarded (receiving tokens) or punished (losing tokens). In all of these tasks, impulsive participants may insufficiently learn from previous loss-trials or series. A probabilistic selection task may also be used to measure impulsivity defined as impaired learning from negative feedback, or (see below) as premature responding under high-conflict conditions (when presented with conflicting positive reward probabilities). Impulsive participants may insufficiently learn from their previous losses and/or respond faster in high-conflict trials.

Delay Discounting (Table 2): Delay discounting tasks may be used to measure impulsivity defined as discounting of larger delayed reward over smaller immediate reward. Examples include the Kirby Delay-Discounting Task (Kirby and MarakoviĆ, 1996). Impulsive participants may impulsively discount future reward, i.e., show increased delay discounting. The Cambridge Gambling Task (Rogers et al., 1999), used by Torta et al. (2012), measures delay aversion, identifying subjects who repeatedly pick the initial bet offered, and results are here presented alongside studies of delay discounting, the measure of impulsive tendencies it most closely resembled.

Inhibitory control (Table 3): Go/No-Go task (Donders, 1969), Stop Signal Task [SST, (Logan and Cowan, 1984)], Status Quo Task (SQT, Fleming et al., 2010) and Stroop test (Stroop, 1935), Simon (Simon and Rudell, 1967). These tasks may be used to measure impulsivity defined as impaired inhibitory control over prepotent motor or cognitive responses. In Go/No-Go, SST and SQT, participants are presented with a stimulus that requires them either to respond (Go) or withhold a response (No-Go/Stop). Impulsive participants may make more commission errors (Go responses on No-go or Stop trials) and/or anticipation errors (responding too fast). SQT is a modified Go/No-Go measuring response inhibition under high conflict. A ball appears either between two lines (Go) or outside the lines (No-Go). High conflict occurs when the ball is almost touching the line. In the Stroop test, words representing colors are written in colors incongruent to the written word, and participants are required to state aloud the ink color as opposed to reading the written word. Impulsive participants may make more commission errors (reporting the word instead of the color). In the Simon task participants respond to visual cues prompting either contra- or ipsilateral movements.

Responding Under High Conflict (Table 4): ILT, Probabilistic selection tasks, delay discounting, and SQT, discussed above, can all be utilized to gauge impulsive behavior under so called “high conflict” scenarios. These are situation where the range of options available for selection are less readily distinguished from one another. Other paradigms have also been used for this purpose, such as an auditory forced choice task (London et al., 2019).

In addition to studies reporting the prevalence of OCD and OCRD before and after STN DBS in PD, we searched for studies measuring OCD-severity using the Maudsley Obsessive-Compulsive Inventory (MOCI, Hodgson and Rachman, 1977) or the Yale-Brown Obsessive- Compulsive Scale (Y-BOCS, Goodman et al., 1989). The MOCI is a self-rated 30-item scale with sub-scores for checking, cleaning, slowness, and doubting. The Y-BOCS is a clinician-rated 10-item scale with sub-scores for obsessions and compulsions.

In addition, we searched for studies examining aspects of compulsivity in PD related STN DBS utilizing one or more of the following paradigms:

Habit learning tasks (Daw et al., 2005; Gillan et al., 2011) measure compulsivity defined as the dominance of habits over goal-directed learning. Participants learn to respond to stimuli with rewarding or negative reinforcing outcomes which are eventually devalued. Compulsive participants keep habitually responding to devalued stimuli, or show more model-free learning (predicted by reinforcement history) than model-based learning (adapted to devaluation).

Perseveration (Table 5): Wisconsin Card Sorting Task (WCST, Grant and Berg, 1948) is a reversal learning task which may be used to measure compulsivity defined as cognitive inflexibility. Cards must be sorted on the basis of either number, form or color with the sorting rule alternating after 10 correct responses, a fact learned by the participant through trial and error. Compulsive participants make more perseverative errors, indicated by two successive sorts on an incorrect dimension. The original Wisconsin Card Sorting Task (WCST) uses 128 response cards, and a Modified Wisconsin Card Sorting Task (MWCST) simplifies the task, using only 48 response cards (Nelson, 1976).

Attentional set shift (Table 6): Trail Making Task (TMT) Part B (Corrigan and Hinkeldey, 1987) may be used to measure compulsivity defined as impaired attentional set-shifting. Participants must draw a line alternating between letters and numbers (A-1-B-2-C-3, etc.). Compulsive individuals tend to have longer completion times due to less attentional flexibility.

We found 12 studies investigating the prevalence of ICDs (gambling, compulsive shopping, binge eating, hypersexuality, punding, DDS) in a total of 582 PD patients pre- and (6–12 months) post STN DBS (Ardouin et al., 1999; Lim et al., 2009; Lhommée et al., 2012; Shotbolt et al., 2012; Eusebio et al., 2013; Kim et al., 2013; Amami et al., 2015; Castrioto et al., 2015; Gee et al., 2015; Merola et al., 2017). The combined prevalence of ICDs in these patients was 28% (N = 162) before STN DBS and 6% (N = 32) after STN DBS (with variable post-surgical LEDD decreases). In the 162 patients that already showed ICDs before DBS, post-surgical improvement of ICDs was observed in 86% (139 patients), including full remission in 68%. Worsening of ICDs after STN-DBS was found in only 3% of all patients (Pallanti et al., 2010; Lhommée et al., 2012). Although new onset of ICDs after STN-DBS was reported in 38 patients, most of these cases were transient (Shotbolt et al., 2012; Kim et al., 2013; Amami et al., 2015). Factors that were associated with ICDs after DBS were personality disorders, dyskinesias and higher post-surgical LEDD.

Subthalamic deep brain stimulation for OCD gained attention after two patients were treated with STN DBS for PD with comorbid OCD (Mallet et al., 2002). Both cases experienced improvement in motor as well as obsessive-compulsive symptoms. Two weeks after the procedure, the patients were free from compulsions, and obsessions improved by 58% in patient 1 and by 64% in patient 2. Since then, the literature on co-morbid OCD and OCDR in patients with PD undergoing STN DBS is surprisingly sparse.