Full Length ArticleThe role of beta-gamma oscillations in unexpected rewards processing
Introduction
Reward processing in humans is carried out by an extensive fronto-subcortical network, composed by several brain structures including the striatum, amygdala, orbitofrontal and insular cortex (Camara et al., 2009, Koob and Volkow, 2010). The existence of such extensive network requires for an integration mechanism that allows the coordination of the different areas involved in it. Brain oscillations seem to be an optimal mechanism for such task (Buzsáki and Draguhn, 2004, Varela et al., 2001). Specifically high frequency oscillations (beta and gamma bands) are key candidates to synchronize these different components as they allow the integration of information across distant brain areas (Colgin et al., 2009, Steriade, 2006, Uhlhaas and Singer, 2006).
In this regard, intracranial recordings on animals have found increase in beta and gamma oscillatory activity in striatum and frontal cortex after actions that were carried out to obtain rewards (Berke, 2009, Courtemanche et al., 2003). In humans, non-invasive electroencephalographic recordings have revealed an increase in the EEG beta band power (Hallschmid et al., 2002) as well as an increase in the beta/theta ratio activity (Schutter and Van Honk, 2005, Snyder and Hall, 2006) during reward processing. In addition, beta-gamma band (20–35 Hz) power increase has been observed 200–400 ms after positive feedback informing about monetary gains using EEG (Cohen et al., 2007, Marco-Pallarés et al., 2008, Marco-Pallarés et al., 2009; see for a recent replication using Magnetoencephalography, Doñamayor et al., 2011) which might be modulated by probability (Cohen et al., 2007) and magnitude of rewards (Marco-Pallarés et al., 2008). In addition, Marco-Pallarés et al. (2009) found a modulation of this response with the COMT Val158Met polymorphism, supporting a possible role of dopamine in this gain related response.
All these studies suggest that beta-gamma oscillatory activity might be an important brain signature of reward-related networks but little is known about the nature of this response or its functional properties. Direct recordings from the Ventral Tegmental Area of awaken monkeys have shown an increase in the dopaminergic activity after improbable rewards (Fiorillo et al., 2003, Schultz et al., 1997, Waelti et al., 2001) or after larger than expected rewards (Tobler etal., 2005). Complementarily, studies in humans have described that some brain areas such as the ventral striatum (Nucleus Accumbens), amygdala and anterior cingulate cortex are selectively activated when a mismatch is detected between the real feedback obtained from an action and the expected one (hereafter referred as prediction error term, PE; Hare et al., 2008, Rutledge et al., 2010, Yacubian et al., 2006). In this context, it has not been appropriately studied which aspects (i.e. probability, magnitude, expected value or prediction error) elicit and modulate beta-gamma oscillatory activity in monetary reward processing. The goal of the present study is to determine the functional significance of beta-gamma power increase after rewards using a gambling Event-Related Potential (ERP) paradigm in which probability and magnitude of rewards and punishments were carefully manipulated.
Section snippets
Subjects
Twenty-six right-handed healthy students participated in the experiment (four men, mean age 25.6 ± 4.8 (S.D.)) for monetary compensation. None of the participants had any history of neurological diseases or substance abuse. Subjects were paid 30 Euros for participation plus/minus what they won/lost in the game respectively. Written consent was obtained prior to the experiment. The experiment was approved by the local ethical committee.
Design
Experimental design is shown in Fig. 1. The experiment
Behavioral results
Participants chose the three cards from left to right in 29.6% (left), 44.3% (middle) and 26.1% (right) of trials. ANOVA showed a significant effect of card location (F(2,38) = 12.61, P = 0.001) and post hoc t-tests showed that subjects chose the middle card significantly more than the left and right cards (for left and middle: t(19) = − 2.97, p < 0.01, for right and middle: t(19) = − 4.55, P < 0.001) while there was no significant difference in choosing left and right cards (t(19) = 1.79, n.s.). The average
Discussion
In the present study we analyzed the involvement of high-frequency brain oscillatory activity in monetary reward processing in humans. In concrete, we tested whether beta-gamma power increase after a positive feedback was modulated by the probability, magnitude or expected value of the monetary outcome. We found a beta-gamma1
Conclusion
The present paper shows that beta-gamma activity might be a brain signature of unexpected gain that might reflect frontostriatal interactions in the reward network. Further studies are needed to delineate the neural network involved in the generation of this response.
Acknowledgments
Supported by the Ramon y Cajal research program awarded to JMP (RYC-2007-01614), Spanish Government grants (MICINN, PSI2008-03901 to ARF and PSI2009-09101 to JMP) and a grant from the Catalan Government (2009 SGR 93).
References (58)
- et al.
Dopamine in motivational control: rewarding, aversive, and alerting
Neuron
(2010) - et al.
Serial, covert shifts of attention during visual search are reflected by the frontal eye fields and correlated with population oscillations
Neuron
(2009) - et al.
Frontal theta links prediction errorsto behavioral adaptation in reinforcement learning
Neuroimage
(2010) - et al.
Reward expectation modulates feedback-related negativity and EEG spectra
Neuroimage
(2007) - et al.
Cortical electrophysiological network dynamics of feedback learning
Trends Cogn. Sci.
(2011) - et al.
EEG synchronization upon reward in man
Clin. Neurophysiol.
(2002) - et al.
Human oscillatory activity associated to reward processing in a gambling task
Neuropsychologia
(2008) - et al.
Genetic variability in the dopamine system (dopamine receptor D4, catechol-O-methyltransferase) modulates neurophysiological responses to gains and losses
Biol. Psychiatry
(2009) - et al.
Attentional control of the processing of neural and emotional stimuli
Brain Res. Cogn. Brain Res.
(2002) - et al.
Size and probability ofrewards modulate the feedback error-related negativity associated with wins but not losses in a monetarily rewarded gambling task
Neuroimage
(2010)
Electrophysiological ratio markers for the balance between reward and punishment
Brain Res. Cogn. Brain Res.
Grouping of brain rhythms in corticothalamic systems
Neuroscience
Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology
Neuron
Brain reward circuitry: insights from unsensed incentives
Neuron
The role of neuronal synchronization in selective attention
Curr. Opin. Neurobiol.
Affective influences on the attentional dynamics supporting awareness
J. Exp. Psychol. Gen.
Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs
Eur. J. Neurosci.
Predictability modulates human brain response to reward
J. Neurosci.
Episodic multiregional cortical coherence at multiple frequencies during visual task performance
Nature
Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease
J. Neurosci.
Neuronal oscillations in cortical networks
Science
Feedback-related negativity codes prediction error but not behavioral adjustment during probabilistic reversal learning
J. Cogn. Neurosci.
Reward networks in the brain as captured by connectivity measures
Front. Neurosci.
Feedback-related negativity codes prediction error but not behavioral adjustment during probabilistic reversal learning
J. Cogn. Neurosci.
Reinforcement learning signals predict future decisions
J. Neurosci.
Frequency of gamma oscillations routes flow of information in the hippocampus
Nature
Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys
J. Neurosci.
Brain oscillatory activity associated with task switching and feedback processing
Cogn. Affect. Behav. Neurosci.
Temporal dynamics of reward processing revealed by magnetoencephalography
Hum. Brain Mapp.
Cited by (108)
Neural correlates of evaluations of non-binary social feedback: An EEG study
2023, International Journal of PsychophysiologyHeart and brain traumatic stress biomarker analysis with and without machine learning: A scoping review
2023, International Journal of PsychophysiologyThe neural mechanism of non-phase-locked EEG activity in task switching
2023, Neuroscience Letters