Novelty seeking can be a positive trait leading to creativity and innovation, but it is also related to increased risk of damaging addictive behaviour. We have assessed novelty seeking with a three armed bandit task, in which novel stimuli were occasionally introduced, replacing choice options from which the participants had been choosing. This allowed us to assess whether or not they would be prone to selecting novel stimuli. We tested 25 non impulsive patients with Parkinson's disease (PD) and 27 PD patients with impulsive compulsive behaviours (ICBs). Both patient groups were examined “on” and “off” dopaminergic medication in a counterbalanced order and their behaviour was compared with 24 healthy controls. We found that PD patients with ICBs were significantly more prone to choose novel options than either non impulsive PD patients or controls, regardless of medication status. Our findings suggest that attraction to novelty is a personality trait in all PD patients with ICBs which is independent of medication status.
Humans and animals are inherently attracted to new stimuli as these can be potentially rewarding (Daffner et al., 1998, Ennaceur and Delacour, 1988 and Hughes, 2007). High novelty seeking is part of adolescence and may help in normal development and the acquisition of independence (Kelley et al., 2004): adults with novelty seeking personality traits on the other hand often have increased impulsivity, addiction, inability to delay gratification, recklessness and aggressive behaviour (Barratt, 1985, Barratt, 1994 and Belin et al., 2008). A subgroup of patients with Parkinson's disease (PD) develop impulsive compulsive behaviours (PD + ICB) in relation to their dopamine replacement therapies. These include pathological gambling, compulsive sexual behaviour and shopping and the inappropriate, excessive overuse of dopaminergic medication (dopamine dysregulation syndrome, DDS) (Evans et al., 2005, Evans et al., 2006 and Voon et al., 2007b). While self-report questionnaires have suggested that the subgroup of PD + ICB patients with DDS (Evans et al., 2005) and those with pathological gambling (Voon et al., 2007b) have high levels of novelty seeking, this has not been formally studied using metric tests.
The trade-off between choosing options of known value and exploring novel options is known as exploration vs. exploitation (Daw et al., 2006). Exploring novel choices and learning the value of stimuli based on reward feedback have been linked to the ventral striatum, the substantia nigra and the ventral tegmental area of the midbrain (Guitart-Masip et al., 2010 and Wittmann et al., 2008) as well as the hippocampus (Guitart-Masip et al., 2010 and Voon et al., 2010). These areas either contain dopamine neurons or receive strong dopaminergic innervation. Additional studies have examined the dopamine link to learning and exploration. For example, behavioural studies in PD have shown that dopamine levels play an important role in reward learning (Cools et al., 2002, Djamshidian et al., 2010, Frank et al., 2004, Seo et al., 2010 and Voon et al., 2010). Complimenting this work, functional magnetic resonance imaging (fMRI) studies in healthy controls and positron emission tomography (PET) studies in PD + ICB patients have localized reward responsivity to the ventral striatum (Evans et al., 2010, O’Doherty et al., 2003, O'Sullivan et al., 2011 and Steeves et al., 2009). An important role for striatal dopamine D2 receptors in the exploration vs. exploitation trade-off has been suggested by genetic studies (Frank et al., 2009). It seems probable therefore that there is an overlap between the networks which mediate reward learning and novelty seeking, and both processes can be conceptualized as assigning value to choice options.
One of the circuits that has been proposed to mediate novelty effects includes the hippocampal projection to the ventral striatum. Specifically, the hippocampus forms a functional loop with the ventral striatum and the mid-brain dopamine neurons. The hippocampus is activated by novel information (all information that is not stored in long term memory) and regulates, via the ventral striatum, dopamine neuron firing rates (Lisman & Grace, 2005). Neuropathological studies have shown that the parahippocampal gyrus is affected in later stages of PD (Braak et al., 2004). Thus, abnormal and increased activity in the ventral striatum might be triggered by earlier neuropathological changes in the hippocampus in PD + ICB patients.
The aim of the present study was to compare novelty seeking between impulsive and non-impulsive PD patients, and also to examine the role of dopaminergic medication on novelty seeking. We hypothesized that PD + ICB as a group would be more novelty seeking than PD − ICB patients on a task which allows for exploration of novel options. We tested PD + ICB and PD patients without ICB (PD − ICB) on and off their dopaminergic medication on a modified “three armed bandit” choice task (Wittmann et al., 2008), where all participants played for real money. We compared the choices of PD − ICB and PD + ICB patients on and off their medication with a group of healthy controls who were matched for age and education to the patients group.
