The Detection of Novelty Relies on Dopaminergic Signaling: Evidence from Apomorphine's Impact on the Novelty N2

Rangel-Gomez, Mauricio; Hickey, Clayton; Amelsvoort, Thérèse van; Bet, Pierre M; Meeter, Martijn

doi:10.1371/journal.pone.0066469

Cited by 29 publications

(21 citation statements)

References 57 publications

(66 reference statements)

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“…This link may in part be mediated by DA release in the cortex, where noradrenergic terminals co-release DA [39]. Indeed, a few studies have reported evidence that DA agents affect the centroparietal P3 to unexpected and novel stimuli, although primarily when these were task-irrelevant [38,85,86]. This link between catecholamine release and the P3 is not exclusive, because the centroparietal P3 is also modulated by pharmacological manipulations of the cholinergic system [87,88].…”

Section: Discussionmentioning

confidence: 99%

“…First, we used the centroparietal P3 component of the EEG as an electrophysiological correlate of outcome-evoked phasic catecholamine release in the cortex [35–38] (but see the Discussion for a competing hypothesis), and examined trial-by-trial relationships between prediction-error magnitude, P3 amplitude and learning rate using multilevel mediation analyses. Second, we examined the relationships between P3 amplitude and two latent variables—capturing the unexpectedness of an outcome and the uncertainty about the outcome-generating process—that together determine learning rate according to a previously established normative model [4,5,21].…”

Section: Introductionmentioning

confidence: 99%

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Catecholaminergic Regulation of Learning Rate in a Dynamic Environment

et al. 2016

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Adaptive behavior in a changing world requires flexibly adapting one’s rate of learning to the rate of environmental change. Recent studies have examined the computational mechanisms by which various environmental factors determine the impact of new outcomes on existing beliefs (i.e., the ‘learning rate’). However, the brain mechanisms, and in particular the neuromodulators, involved in this process are still largely unknown. The brain-wide neurophysiological effects of the catecholamines norepinephrine and dopamine on stimulus-evoked cortical responses suggest that the catecholamine systems are well positioned to regulate learning about environmental change, but more direct evidence for a role of this system is scant. Here, we report evidence from a study employing pharmacology, scalp electrophysiology and computational modeling (N = 32) that suggests an important role for catecholamines in learning rate regulation. We found that the P3 component of the EEG—an electrophysiological index of outcome-evoked phasic catecholamine release in the cortex—predicted learning rate, and formally mediated the effect of prediction-error magnitude on learning rate. P3 amplitude also mediated the effects of two computational variables—capturing the unexpectedness of an outcome and the uncertainty of a preexisting belief—on learning rate. Furthermore, a pharmacological manipulation of catecholamine activity affected learning rate following unanticipated task changes, in a way that depended on participants’ baseline learning rate. Our findings provide converging evidence for a causal role of the human catecholamine systems in learning-rate regulation as a function of environmental change.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Catecholaminergic Regulation of Learning Rate in a Dynamic Environment

et al. 2016

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“…The neural basis of the reward-related enhancement of cognitive control may rely on dopaminergic pathways that are known to be involved in both reward processing [35–38] and conflict processing [39, 40]. Interestingly, processing of novel information was also shown to activate dopaminergic pathways [41, 42]. Therefore, manipulating stimulus’ novelty may support response selection and inhibition through the dopaminergic pathways [3, 4].…”

Section: Discussionmentioning

confidence: 99%

Picture Novelty Influences Response Selection and Inhibition: The Role of the In-Group Bias and Task-Difficulty

et al. 2016

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The human visual system prioritizes processing of novel information, leading to faster detection of novel stimuli. Novelty facilitates conflict resolution through the enhanced early perceptual processing. However, the role of novel information processing during the conflict-related response selection and inhibition remains unclear. Here, we used a face-gender classification version of the Simon task and manipulated task-difficulty and novelty of task-relevant information. The novel quality of stimuli was made task-irrelevant, and an in-group bias was tightly controlled by manipulation of a gender of picture stimuli. We found that the in-group bias modulated the role of novelty in executive control. Novel opposite-sex stimuli facilitated response inhibition only when the task was not demanding. By contrast, novelty enhanced response selection irrespective of the in-group factor when task-difficulty was increased. These findings support the in-group bias mechanism of visual processing, in cases when attentional resources are not limited by a demanding task. The results are further discussed along the lines of the attentional load theory and neural mechanisms of response-inhibition and locomotor activity. In conclusion, our data showed that processing of novel information may enhance executive control through facilitated response selection and inhibition.

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“…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 animals (Costa et al, 2014). Furthermore, genetic studies have emphasised the importance of D2 receptors in the regulation of exploration versus exploitation behaviour (Frank & Hutchison, 2009).…”

Section: Introductionmentioning

confidence: 99%

The value of novelty in schizophrenia

Martinelli

Rigoli

Averbeck

et al. 2018

Schizophrenia Research

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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.

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The Detection of Novelty Relies on Dopaminergic Signaling: Evidence from Apomorphine's Impact on the Novelty N2

Cited by 29 publications

References 57 publications

Catecholaminergic Regulation of Learning Rate in a Dynamic Environment

Catecholaminergic Regulation of Learning Rate in a Dynamic Environment

Picture Novelty Influences Response Selection and Inhibition: The Role of the In-Group Bias and Task-Difficulty

The value of novelty in schizophrenia

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