The value of novelty in schizophrenia

Abstract

Influential models of schizophrenia suggest that patients experience incoming stimuli as excessively novel and motivating, with important consequences for hallucinatory experience and delusional belief. However, whether schizophrenia patients exhibit excessive novelty value and whether this interferes with adaptive behaviour has not yet been formally tested. Here, we employed a three-armed bandit task to investigate this hypothesis. Schizophrenia patients and healthy controls were first familiarised with a group of images and then asked to repeatedly choose between familiar and unfamiliar images associated with different monetary reward probabilities. By fitting a reinforcement-learning model we were able to estimate the values attributed to familiar and unfamiliar images when first presented in the context of the decision-making task. In line with our hypothesis, we found increased preference for newly introduced images (irrespective of whether these were familiar or unfamiliar) in patients compared to healthy controls and this to correlate with severity of hallucinatory experience. In addition, we found a correlation between value assigned to novel images and task performance, suggesting that excessive novelty value may interfere with optimal learning in patients, putatively through the disruption of the mechanisms regulating exploration versus exploitation. Our results suggest excessive novelty value in patients, whereby even previously seen stimuli acquire higher value as the result of their exposure in a novel context – a form of ‘hyper novelty’ which may explain why patients are often attracted by familiar stimuli experienced as new.

Introduction

As humans, we are often faced with the dilemma of choosing between a familiar and novel option; whether to order ‘the usual’ or try a new dish in a restaurant, book last year's holiday destination or go somewhere new are all examples where the values of the known and the unknown are weighted and compared with each other. The choice is not inconsequential as the two options hold different motivational value and satisfy different goals: exploring novel options permits the acquisition of new information in order to optimise behaviour in the long run, whereas pursuing options with known values facilitates the efficient exploitation of available information. It has been argued that humans have developed mechanisms aimed at increasing the value of novel stimuli as a way to promote exploration of unknown options (Kakade and Dayan, 2002). However, high novelty value and novelty-seeking behaviour are only appropriate if the balance between exploration and exploitation is kept at optimal levels (Pezzulo et al., 2013), as dysfunctions in this regulatory mechanism may lead to motivational disturbance and maladaptive behaviour (Averbeck, 2015, Friston et al., 2015).

In schizophrenia, several considerations hint that there may be an important deficit in the balance between the value attributed to old and novel stimuli. Within a Bayesian inference framework, influential models of schizophrenia propose that patients give relatively excessive weight to incoming sensory evidence compared to prior beliefs, resulting in heightened sense of novelty and an on-going state of surprise (Adams et al., 2013, Fletcher and Frith, 2009). Other theories have also emphasised patients' alterations in novelty processing as central to the disorder, suggesting that key symptoms, such as delusions and hallucinations, may be consequent upon aberrant salience attribution associated with novelty processing. This is supported by observations of patients with psychosis perceiving routine stimuli as novel-like and excessively engaging, with a consequent elaboration of the importance of this sense of novelty into delusional belief and hallucinatory experience (Kapur, 2003, Kapur et al., 2005). Hence, such theories propose that patients may exhibit motivational dysfunctions as the result of aberrant novelty processing, but the nature of this aberrance remains unclear.

That there is an imbalance in the proper allocation of novelty value in schizophrenia is further supported by evidence pointing towards a link between novelty-seeking traits and several behaviours such as excessive drug (Kim et al., 2007) and alcohol consumption (Dervaux et al., 2010), impulsivity (Ouzir, 2013) and violent behaviour (Fresán et al., 2007). Novelty-seeking has also been associated with non-adherence to medication (Margetić et al., 2011) and increased hospital admissions (albeit only in males; Miralles et al., 2014). In line with models of motivational regulation, these findings suggest that excessive attraction towards novel stimuli may disrupt motivational regulation and thus interfere with optimal decision-making and behaviour in patients affected by schizophrenia.

However, whether patients exhibit higher novelty-seeking traits relative to healthy controls remains unclear, as effects in both directions have been reported (Ohi et al., 2012). It is important to clarify that that the existing studies relied on self-report measures, which suffer from well-recognised limitations (Martinelli et al., 2013, Wilson and Dunn, 2004). In the context of novelty value investigations, the use of self-reports may be particularly misleading, as many of the questions used to assess novelty-seeking behaviour are not relevant to the life style of most patients. Thus, occasional observations of reduced novelty-seeking in patients may be merely reflecting the lack of their engagement in the activities used to assess this trait. It would be much more informative to have a direct on-line behavioural assessment in determining the presence of novelty-seeking alterations in the illness.

Additional support for the involvement of novelty processing in schizophrenia comes from evidence that dopamine, known to play a crucial role in the neurobiological substrate of schizophrenia, may crucially modulate novelty value in healthy individuals. In line with this, a recent study found a correlation between brain activity in the midbrain and ventral striatum, and value attributed to novelty while engaging in a decision-making task, as well as between the same brain areas and novelty-seeking traits (Wittmann et al., 2008). Moreover, pharmacological manipulation studies observed a correlation between increase in dopamine levels and novelty detection in humans (Rangel-Gomez et al., 2013) as well as novelty- seeking in humans (Rigoli et al., 2016) and animals (Costa et al., 2014). Furthermore, genetic studies have emphasised the importance of D2 receptors in the regulation of exploration versus exploitation behaviour (Frank and Hutchison, 2009). In schizophrenia, evidence of dopamine unbalance playing a key role in the illness (Howes and Kapur, 2009) suggests that patients may experience excessive novelty value as a consequence of their dopaminergic dysregulation.

Despite evidence described above, novelty salience dysfunctions in schizophrenia have not yet been formally tested. In the present study, we studied novelty value in schizophrenia with an armed bandit task (Daw et al., 2006), which has been successfully employed for the investigation of novelty-seeking behaviour in healthy individuals (Wittmann et al., 2008) and those affected by Parkinson's disease (Djamshidian et al., 2011). We tested the hypotheses that: a) patients would exhibit enhanced novelty-seeking compared to healthy controls; b) altered novelty processing in patients would interfere with their decision-making leading to sub-optimal performance; and c) altered novelty value would be associated with severity of psychotic symptoms, namely hallucinations and delusions.