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Article  |   February 2011
Dopaminergic stimulation enhances confidence and accuracy in seeing rapidly presented words
Author Affiliations
  • Hans C. Lou
    Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark
    Institute for Preventive Medicine, University of Copenhagen, Copenhagen, Denmarkhttp://www.ipm.regionh.dkhl@ipm.regionh.dk
  • Joshua C. Skewes
    Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmarkjosh.skewes@gmail.com
  • Kristine Rømer Thomsen
    Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmarkkristineroemerthomsen@hotmail.com
  • Morten Overgaard
    CNRU Hammel Neurorehabilitation and Research Center, Aarhus University Hospital, Aarhus, Denmark
    CNRU Department of Communication and Psychology, Aalborg University, Aalborg, Denmarkmorten.overgaard@hammel.rm.dk
  • Hakwan C. Lau
    Department of Psychology, Columbia University, New York, NY, USAhakwan@gmail.com
  • Kim Mouridsen
    Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmarkkim@cfin.dk
  • Andreas Roepstorff
    Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmarkandreas@pet.au.dk
Journal of Vision February 2011, Vol.11, 15. doi:10.1167/11.2.15
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      Hans C. Lou, Joshua C. Skewes, Kristine Rømer Thomsen, Morten Overgaard, Hakwan C. Lau, Kim Mouridsen, Andreas Roepstorff; Dopaminergic stimulation enhances confidence and accuracy in seeing rapidly presented words. Journal of Vision 2011;11(2):15. doi: 10.1167/11.2.15.

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Abstract

Liberal acceptance, overconfidence, and increased activity of the neurotransmitter dopamine have been proposed to account for abnormal sensory experiences, for instance, hallucinations in schizophrenia. In normal subjects, increased sensory experience in Yoga Nidra meditation is linked to striatal dopamine release. We therefore hypothesize that the neurotransmitter dopamine may function as a regulator of subjective confidence of visual perception in the normal brain. Although much is known about the effect of stimulation by neurotransmitters on cognitive functions, their effect on subjective confidence of perception has never been recorded experimentally before. In a controlled study of 24 normal, healthy female university students with the dopamine agonist pergolide given orally, we show that dopaminergic activation increases confidence in seeing rapidly presented words. It also improves performance in a forced-choice word recognition task. These results demonstrate neurotransmitter regulation of subjective conscious experience of perception and provide evidence for a crucial role of dopamine.

Introduction
The relationship between conscious experience of perception and neural events is a key issue in modern neuroscience (Crick & Koch, 2003). Although we lack a complete knowledge of the function of consciousness to help us in understanding its relationship to brain function, there is good reason to believe that consciousness is involved in the higher order gating of sensory inputs. Dopaminergic neurons to the striatum have been proposed to play a determining role in gating of sensory inputs (Horvitz, 2002), and enhanced sensory experience during Yoga Nidra meditation is linked to dopamine release in nucleus accumbens of the ventral striatum (Kjaer et al., 2002), suggesting that dopamine may be active in regulating conscious experience. One way to understand this idea is to approach conscious experience as a form of higher order signal detection. On this approach, conscious experience is determined by the setting of a criterion for when the sensory signal-to-noise ratio warrants confidence that the stimulus represents something real (Lau, 2007). Consistent with this approach, work on schizophrenia shows not only that patients with auditory hallucinations have enhanced sensitivity to speech stimuli, but they also set more liberal criteria for deciding that a perceived event is an actual stimulus. Psychotic symptoms may, accordingly, be explained at least partly as a result of setting too liberal a signal-to-noise criterion leading to confusion between perception and imagination (Moritz & Larøi, 2008; Vercammen, de Haan, & Aleman, 2008; Winterer et al., 2000). Abnormally up-regulated dopaminergic neurotransmission (Gjedde & Wong, 2001; Kroener, Chandler, Phillips, & Seamans, 2009) may be one of the mechanisms responsible for this difference, with an effect of dopamine on the cellular level being to influence the signal-to-noise ratio (Kiyatkin & Rebec, 1996, 1999; Williams & Goldman-Rakic, 1995; Winterer et al., 2000). Functional brain imaging has established that abnormal conscious experiences, like hallucinations, are associated with abnormal dopaminergic neurotransmission. For instance, striatal dopamine transporter availability is inversely correlated with hallucinations (Schmitt et al., 2006). Accordingly, acute psychosis is generally considered a consequence of a hyperdopaminergic state (Howes & Kapur, 2009; Laruelle & Abi-Dargham, 1999). 
There is therefore good reason to believe that dopamine is not only correlated with subjective conscious experience of perception, but that it plays a real causal role. Dopaminergic agents have even been reported to be effective in regulating the state of consciousness by awakening patients suffering from severe disorders of consciousness, like the vegetative state or the minimally conscious state (Matsuda, Komatsu, Yanaka, & Matsumura, 2005). This led us to think that dopamine may regulate not only performance but also acknowledged confidence in subjective conscious experiences of visual perception. 
We tested this hypothesis in a controlled, between-subjects experiment that directly examined the effect of increasing dopamine activation on confidence in seeing words, a valid measure of stimulus awareness (Kunimoto, Miller, & Pashler, 2001; Szczepanowski & Pessoa, 2007; Weiskrantz, Barbur, & Sahraie, 1995; Wilimzig, Tsuchia, Fahle, Einhäuser, & Koch, 2008). Participants were asked to perform a task requiring two-alternative match-to-sample response, with each trial followed by a confidence rating. The quality of confidence in predicting performance in recognition of visually presented words was assessed with a dual choice behavioral response. 
Participants
Thirty-one prospective participants were screened for the study. Seven were not included due to practical obstacles, acute or chronic disease, or withdrawal of initial consent. The remaining 24 participants were all students at the University of Aarhus. All participants were female and aged between 20 and 30 years. All participants were right-handed native Danish speakers. All participants were of good health. Neuropsychiatric disorders including head trauma, pregnancy, and drug use, except for anticonception, were ruled out by a screening interview by an MD, board qualified in neurology. The participants were asked not to drink coffee or alcohol in the morning before the investigation. The study had been approved by the Ethical Committee for the Central Denmark region and was carried out according to the Helsinki Declaration after individual oral and written consents. 
Design
The study was a double-blind investigation of 24 participants, allocated randomly to two groups by flip of a coin. Twelve participants received 0.1 mg of pergolide orally, and 12 received a placebo. Drug and placebo were given approximately 2.5 h before the behavioral task. In both groups, a peripherally active D2 dopamine antagonist domperidone was given orally. This was done 12, 2, and 0.5 h (10 mg × 3) before drug or placebo to counteract nausea and vomiting, which are common side effects of pergolide. Domperidone has only minimal effect on the central nervous system, as it does not pass the blood–brain barrier to any appreciable degree (Reddymasu, Soykan, & McCallum, 2007). One participant was excluded due to severe side effects of pergolide. The remaining eleven tolerated the drug well. 
Pergolide was used as a dopaminergic agonist, because this drug has been well studied in a number of cognitive tasks, in particular in working memory (Gibbs & D'Esposito, 2006; Müller, von Cramon, & Pollmann, 1998). Drug dosages and timing were carried out as described by Müller et al. The only difference was that they used a repeated measures design, while the present study used a between-subjects design. This was done to control for learning effects associated with the task. 
Behavioral task
Stimuli were masked presentations of three- and four-letter randomly chosen monosyllabic Danish words in common usage. Masks were random combinations of Cyrillic consonants, matched in length to the word. Stimuli were presented on an LCD monitor positioned 60 cm from the participant. Stimulus size was approximately 4° × 10° of visual angle. Each trial started with a fixation cross, presented for 500 ms. This was immediately followed by presentation of the word for 33 ms, 50 ms, or 66 ms, which was immediately followed by a mask presented for 200 ms. Forty trials were presented for each word presentation time, giving a total of 120 trials. The word presentation time used on each trial was randomized. Each word was presented only once (Figure 1d). 
Figure 1
 
Effect of dopaminergic activation on confidence in seeing words and on accuracy in word recognition task. (a) Increase in subjective rating of confidence (scale 0–3) for words presented at 33 ms, 50 ms, and 66 ms (means and standard deviations of means, p = 0.0018). (b) Increase in accuracy (percentage of correct responses, in word recognition task by forced choice, one distractor). Expectation from chance: 50%. Note ceiling effect (p = 0.006). (c) All observations of correct answers as a function of confidence, showing a significant effect (p < 0.0001, regression with random effect). The pergolide-treated group and the placebo groups had identical regression lines statistically, in spite of slight difference on visual inspection. (d) Experimental time line.
Figure 1
 
Effect of dopaminergic activation on confidence in seeing words and on accuracy in word recognition task. (a) Increase in subjective rating of confidence (scale 0–3) for words presented at 33 ms, 50 ms, and 66 ms (means and standard deviations of means, p = 0.0018). (b) Increase in accuracy (percentage of correct responses, in word recognition task by forced choice, one distractor). Expectation from chance: 50%. Note ceiling effect (p = 0.006). (c) All observations of correct answers as a function of confidence, showing a significant effect (p < 0.0001, regression with random effect). The pergolide-treated group and the placebo groups had identical regression lines statistically, in spite of slight difference on visual inspection. (d) Experimental time line.
Following each trial, participants were asked to use a four-point Likert scale to rate how confident they were that they had seen the stimulus word (confidence response). Following this, the stimulus word was presented alongside a distracter word. As with the stimulus words, each distracter word was only presented once, and no distracter word was ever presented as a stimulus. The locations of the stimulus and the distracter words (i.e., left or right of the screen) were randomized across trials. Participants were asked to use a button press to determine which of the two words was the stimulus (discrimination response). The confidence task was given first to avoid anchoring effects associated with the response on the discrimination response. Participants were given unlimited time to make all of their responses and were asked to prioritize accuracy over speed. Each testing sessions started with ten practice trials to familiarize participants with the stimuli. 
Results
A 2 × 3 mixed model ANOVA on confidence ratings revealed significant main effects of presentation time [F(2, 44), = 178.1, p < 0.0001] and drug treatment [F(1, 21), = 12.8, p = 0.0018] with participants who received pergolide scoring 44%, 28%, and 19% higher confidence ratings compared to placebo at the three presentation times (Figure 1a). This result shows that pergolide increases subjective confidence significantly. 
A 2 × 3 mixed model ANOVA on discrimination performance revealed significant main effects of presentation time [F(2, 44), = 132.5, p < 0.0001] and drug treatment [F(1, 21), = 9.3, p = 0.006] and a significant interaction between the two [F(2, 44), = 3.54, p = 0.038], with participants who received placebo showing improved accuracy in the word recognition response by 15%, 15%, and 1% for the three presentation times (Figure 1b). This result shows that pergolide increases objective retrieval significantly. 
Figure 1c shows correct answers as a function of subjective confidence. This relationship is highly significant (p < 0.0001, regression with random effect). The treated group and the placebo group had statistically the same interaction between subjective confidence and objective accuracy, in spite of a slight difference on visual inspection of the regression lines. This impression is presumably due to the ceiling effect visible in Figure 1b. The interaction was linear throughout the presentation times, indicating a proportional effect of presentation times on confidence and accuracy. 
Discussion
Our study is the first experimental study to show neurotransmitter regulation of confidence of subjective experience and provides evidence for a crucial role of dopamine. We realize that although pergolide is a strong dopaminergic agonist stimulating D1, D2, and D3 receptors, this effect is not specific. A serotonergic agonist effect is also present, with stimulation of 5-HT1A and 5-HT2A receptors (Millan et al., 2002). However, the observed stimulating effect of pergolide medication on confidence in conscious experience is unlikely to be due to stimulation of serotonergic receptors, because the selective 5-HT1A/2A receptor agonist psilocybin decreases conscious experience of time perception and working memory, and because psilocybin medication induces drowsiness, fatigue, introversion dreaming, and lack of concentration (Wittmann et al., 2007). Nevertheless, an effect of serotonin on confidence in conscious experience or the ability to discriminate a stimulus cannot be entirely excluded. Further experiments with other agonists and antagonists are therefore warranted. 
Usually cognitive performance varies with subjective confidence rating (Kolb & Braun, 1995; Morgan, Mason, & Solomon, 1997). This is also the case here (cf. Figure 1c). The close relationship between confidence rating and performance on a forced-choice word recognition task raises the question of whether their increase with dopaminergic activation could occur via the well-known effects on attention (Iversen & Iversen, 2007) or working memory (Müller et al., 1998). Available evidence speaks against this idea. Authors from the Division of Biology, California Institute of Technology have recently described a three-way interaction between attention, subjective experience, and objective performance (Wilimzig et al., 2008). They reported that spatial attention increases performance but not subjective confidence in a discrimination task. No matter whether the manipulation of attention resulted in a weak or a substantial difference in performance, confidence ratings for attended and unattended stimuli were approximately constant. 
Dopaminergic stimulation with pergolide has been shown repeatedly to increase working memory (e.g., Gibbs & D'Esposito, 2006; Müller et al., 1998). Working memory enhancement is therefore hypothetically a second possible explanation of the effect of dopaminergic stimulation on confidence and performance. Yet, empirical data on the interaction between memory and judgment suggest that this is not likely: In an extensive analysis of the literature, it was noted that judgment is based on either memories or online presentation of the task. It was found that judgment is typically independent on memory when information for judgment is presented synchronously with the task (Anderson & Hubert, 1963; Hastie & Park, 1986). This is the case in the present study. 
Finally, dopaminergic stimulation is known to improve mood (Wise & Bozarth, 1985), which, again, may improve retrieval performance (Barros et al., 2001). This suggests that dopaminergic activation exerts its influence on performance at least partially via its effect on mood. Striatal dopamine release is associated with the feeling of saliency and reward (Pessiglione, Seymour, Flandin, Dolan, & Frith, 2006). A link between subjective confidence and reward would be expected if the main cognitive function of subjective confidence were to make adaptive control of behavior possible. This is a widely held belief (Cleeremans, 2001). The reward system would then be able to add salience (“wanting incentives”, Berridge & Robinson, 1998) to experiences to guide processes of learning and adaptation. Recently, direct evidence has demonstrated the link between reward maximization and human detection behavior and confidence (Navalpakkam, Koch, & Perona, 2009). In fact, humans are quickly able to optimize reward-harvesting decisions by combining the feeling of ease of detection (i.e., “confidence”) with the value of the target (Navalpakkam, Koch, Rangel, & Perona, 2010). Expectation of reward therefore predicts both confidence and performance. A link between reward and awareness is further suggested by the activation of key cortical regions in the paralimbic reward system, including orbito-frontal, anterior cingulate, and posterior cingulate/medial parietal regions (Liu, Hairston, Schrier, & Fan, 2010) with conscious awareness of visually presented words (Kjaer, Nowak, Kjaer, Lou, & Lou, 2001). 
To be effective in confidence in conscious experience, dopaminergic release must occur early in visual processing, and early release is supported by recent experimental findings: The midbrain superior colliculus is a primary visual structure, specialized for the detection of rewarding (Comoli et al., 2003), unexpected (Dommett et al., 2005), and salient (Redgrave, Prescott, & Gurney, 1999) stimuli. It is reached directly by visual pathways and has direct connections to the substantia nigra pars compacta, the origin of nigro-striatal fibers innervating the striatum and limbic structures (Dommett et al., 2005). The latency of this circuitry is very short, approximately 100 ms. In this time, dopaminergic neurons respond to a visual event even before the onset of a visual saccade, and before the stimulus is in focus (Redgrave et al., 1999). The effect of the activity in the circuitry is therefore pre-attentive. 
With dopamine as a key to confidence in subjective experience, dopamine is not only a mediator of contextually meaningful information but may also in excess be a generator of excessive confidence of that one's interpretation of the world is correct, leading to hallucinations (Schmitt et al., 2006). 
Acknowledgments
The authors are grateful for comments by Professor J. Scheel-Krüger and Professor Chris Frith. 
Commercial relationships: none. 
Corresponding author: Hans C. Lou. 
Email: hl@ipm.regionh.dk. 
Address: Center of Functionally Integrative Neuroscience, Aarhus University, DK 8000 Aarhus C, Denmark. 
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Figure 1
 
Effect of dopaminergic activation on confidence in seeing words and on accuracy in word recognition task. (a) Increase in subjective rating of confidence (scale 0–3) for words presented at 33 ms, 50 ms, and 66 ms (means and standard deviations of means, p = 0.0018). (b) Increase in accuracy (percentage of correct responses, in word recognition task by forced choice, one distractor). Expectation from chance: 50%. Note ceiling effect (p = 0.006). (c) All observations of correct answers as a function of confidence, showing a significant effect (p < 0.0001, regression with random effect). The pergolide-treated group and the placebo groups had identical regression lines statistically, in spite of slight difference on visual inspection. (d) Experimental time line.
Figure 1
 
Effect of dopaminergic activation on confidence in seeing words and on accuracy in word recognition task. (a) Increase in subjective rating of confidence (scale 0–3) for words presented at 33 ms, 50 ms, and 66 ms (means and standard deviations of means, p = 0.0018). (b) Increase in accuracy (percentage of correct responses, in word recognition task by forced choice, one distractor). Expectation from chance: 50%. Note ceiling effect (p = 0.006). (c) All observations of correct answers as a function of confidence, showing a significant effect (p < 0.0001, regression with random effect). The pergolide-treated group and the placebo groups had identical regression lines statistically, in spite of slight difference on visual inspection. (d) Experimental time line.
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