Human oscillatory activity associated to reward processing in a gambling task
Introduction
In order to successfully navigate through a busy day, we need to constantly assess the values and uncertainties attached to different options and to adapt our behavior according to the outcome of an action which might or might not match our predictions and hopes. The function of positive (rewards) and negative feedback signals (punishments) in this scenario is to guide behavior and to mediate learning (Schultz, 2006). The brain network activated in reward processing comprises the orbitofrontal cortex, amygdala, ventral striatum/nucleus accumbens, prefrontal cortex and anterior cingulate cortex (Delgado, Nystrom, Fissell, Noll, & Fiez, 2000; Gottfried, O’Doherty, & Dolan, 2003; Knutson, Fong, Bennett, Adams, & Hommer, 2003; Knutson, Westdorp, Kaiser, & Hommer, 2000; O’Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001). However, although the neural circuit involved in reward processing is quite well defined, the specific roles of each region and the integration of information in this circuit are not well understood.
Several authors have proposed that in order to integrate a disparate number of different rewards the brain uses a common network that converges in a final pathway that informs about the nature of the reward (comparison process) and about the possible courses of action in the future (Montague & Berns, 2002; Shizgal, 1997). Neurophysiological studies in animals revealed dopaminergic neurons in the midbrain projecting, among other regions, to the ventral striatum responding selectively to unpredicted events: (i) they are mostly responsive to appetetive events that are better than predicted, (ii) they do not respond to well-predicted rewards, and (iii) a negative signal (i.e. decreased activity) is elicited when an appetetive event is worse than predicted (Mirenowicz & Schultz, 1994; Schultz, Dayan, & Montague, 1997; Tremblay & Schultz, 2000; for similar results in humans: Berns, McClure, Pagnoni, & Montague, 2001; O’Doherty et al., 2001). The pattern observed in these neurons contrasts to that observed in prefrontal, anterior, and posterior cingulate cortex neurons which exhibit only a unidirectional “error signal” (Ito, Stuphorn, Brown, & Schall, 2003; McCoy, Crowley, Haghighian, Dean, & Platt, 2003; Watanabe, 1989, however see Kim, Shimojo, & O’Doherty, 2006; Tom, Fox, Trepel, & Poldrack, 2007).
In non-invasive electrophysiological studies in humans using event-related brain potentials (ERPs), a similar “error signal” has been observed emanating from the medial prefrontal cortex (Carter et al., 1998, Ullsperger and von Cramon, 2001). Frontocentral negativity, called error-related negativity (ERN, Falkenstein, Hohnsbein, Hoormann, & Blanke, 1990; Gehring, Goss, Coles, Meyer, & Donchin, 1993) has been recorded after performance errors. In addition, a similar medial frontal negativity (MFN) has also been observed after feedback informing that a response had been incorrect (Holroyd & Coles, 2002; Muller, Moller, Rodriguez-Fornells, & Munte, 2005) or after feedback informing about the amount of money lost in a gambling task (Gehring & Willoughby, 2002). Gehring and Willoughby (2004) have used a Morlet wavelet-based time–frequency analysis of the average ERN and MFN components to analyze oscillatory activity underlying these ERP responses. A theta oscillatory response (4–7 Hz) with a maximum at midline electrodes was found in relation to both ERP components. This result corroborated previous time–frequency studies of the ERN component (Luu, Tucker, & Makeig, 2004; Yordanova, Falkenstein, Hohnsbein, & Kolev, 2004). As the scalp distribution of the theta oscillatory activity was slightly lateralized to the right and more anterior than for the MFN compared to the ERN component, their neural generators may be partially distinct (Nieuwenhuis, Slagter, von Geusau, Heslenfeld, & Holroyd, 2005; Muller et al., 2005). Luu and Tucker (2001) have suggested that the midline theta oscillatory process underlying the ERN component may reflect the broad coordination of several brain regions (which include the anterior cingulate cortex and several subcortical regions) that participate in the action regulation system. This system might be involved in learning the appropriateness of a behavior in a specific context, monitoring the outcome of actions and switching to a different behavior when unexpected outcomes occur.
One important limitation of the Gehring and Willoughby (2004) study is that the time–frequency analysis was applied only to averaged ERP activity, which only accounts for the electrical activity reflected by the evoked potential. In contrast, single trial time–frequency analysis provides information that cannot be gleaned from averaged ERPs or time–frequency analysis of average data (see, for example, Makeig et al., 2002; Tallon-Baudry, Bertrand, Delpuech, & Pernier, 1997): (i) there is no information loss due to the averaging process in the time or spectral domains; (ii) it is possible to study systematic variations between single trials, and (iii) changes of power of non-phase-locked activity in a given frequency band can be assessed (Tallon-Baudry et al., 1997), which is especially important for higher frequencies. Thus, fine-grained wavelet-based time–frequency analysis could help to solve the question as to why no specific electrophysiological effects have been recorded for affirmative feedback information, monetary gains or correct responses using standard time–domain ERP analysis or time–frequency analysis applied to averaged ERP data. In the present study we therefore employed trial-by-trial wavelet-based time–frequency analysis in addition to standard ERP analysis in a simplified version of the gambling task developed by Gehring and Willoughby (2002).
Section snippets
Participants
Twenty-five right-handed healthy undergraduate psychology students of the University of Barcelona participated in the experiment (seven men, mean age 23.7 ± 5.4 (S.D.)) for monetary compensation. Written consent was obtained prior to the experiment. The experiment was approved by the local ethical committee.
Design
We used a simplified version of the gambling task (Gehring & Willoughby, 2002) in which valence (reward/monetary gain or punishment/monetary loss) and correctness (correct or incorrect choice)
Results
The mean gain of the participants after performing the 768 trials was 7.4 ± 467.3 points. Ten participants ended the experiment gaining some points, 14 participants lost points and one participant ended the experiment with 0 points.
Discussion
Rewards and punishments are major forces in the modification of behavior. Using event-related brain potentials in the human, a negative component (MFN) has been observed for feedback information signaling negative outcomes (e.g. monetary loss; Gehring & Willoughby, 2002; Holroyd & Coles, 2002; Muller et al., 2005, Nieuwenhuis et al., 2005). By implementing trial-by-trial time–frequency analysis we were able to study the relationship between oscillatory activity and the processing of reward and
Conclusion
Time–frequency analysis of feedback related activity revealed two different oscillatory responses. First, a frontocentral theta component was seen in response to negative feedback, which underlies the previously described medial frontal ERP negativity. By contrast, a high-frequency frontocentral beta response was associated with positive feedback (monetary gains), whose function might be to functionally couple different brain areas during reward processing.
Acknowledgements
This research was supported by research grants of Spanish Government (SEJ2005-06067/PSIC to ARF and SEC2001-3821C0501 to AAP), the Ramon y Cajal research program and the Volkswagenstiftung to ARF and TFM. TFM is also supported by the DFG and the BMBF. Special thanks to Estela Camara, Anna Mestres-Missé and Lluis Fuentemilla for their technical help and comments at various stages of the project.
References (56)
- et al.
Functional imaging of neural responses to expectancy and experience of monetary gains and losses
Neuron
(2001) Theta oscillations in the hippocampus
Neuron
(2002)- et al.
Reward expectation modulates feedback-related negativity and EEG spectra
Neuroimage
(2007) - et al.
The feedback-related negativity reflects the binary evaluation of good versus bad outcomes
Biological Psychology
(2006) - et al.
EEG synchronization upon reward in man
Clinical Neurophysiology
(2002) - et al.
Hemodynamic correlates of EEG: A heuristic
Neuroimage
(2005) - et al.
A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: Characterization with rapid event-related fMRI
Neuroimage
(2003) - et al.
FMRI visualization of brain activity during a monetary incentive delay task
Neuroimage
(2000) - et al.
Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study
Neuron
(1998) - et al.
Regulating action: Alternating activation of midline frontal and motor cortical networks
Clinical Neurophysiology
(2001)
Frontal midline theta and the error-related negativity: Neurophysiological mechanisms of action regulation
Clinical Neurophysiology
Saccade reward signals in posterior cingulate cortex
Neuron
Neural economics and the biological substrates of valuation
Neuron
Brain potentials related to self-generated and external information used for performance monitoring
Clinical Neurophysiology
Electrophysiological ratio markers for the balance between reward and punishment
Brain Research Cognitive Brain Research
Neural basis of utility estimation
Current Opinion in Neurology
Grouping of brain rhythms in corticothalamic systems
Neuroscience
Theta EEG dynamics of the error-related negativity
Clinical Neurophysiology
Subprocesses of performance monitoring: A dissociation of error processing and response competition revealed by event-related fMRI and ERPs
Neuroimage
The appropriateness of behavioral responses coded in post-trial activity of primate prefrontal units
Neuroscience Letter
Parallel systems of error processing in the brain
Neuroimage
Predictability modulates human brain response to reward
Journal of Neuroscience
Conflict monitoring and cognitive control
Psychological Review
Episodic multiregional cortical coherence at multiple frequencies during visual task performance
Nature
Anterior cingulate cortex, error detection, and the online monitoring of performance
Science
Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys
Journal of Neuroscience
Tracking the hemodynamic responses to reward and punishment in the striatum
Journal of Neurophysiology
Effects of errors in choice reaction task on the ERP under focused and divided attention
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