Research reportBrain signatures of monetary loss and gain: Outcome-related potentials in a single outcome gambling task
Introduction
In recent years, there has been a focused research interest to examine the event-related potential (ERP) components in gambling-type paradigms. This trend is a continuation of numerous studies on error-related negativity (ERN or Ne), a sharp negative deflection in the ERP waveform with a frontocentral scalp distribution peaking around 100 ms following an erroneous response in choice-reaction tasks [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11], [12], [13], [14]. Medial frontal negativity (MFN), a closely related phenomenon to ERN, was recently reported by Gehring and Willoughby [15]. MFN occurred around 250 ms after outcome stimuli that informed human participants about gains and losses in a two-choice two-outcome (TCTO) gambling task. While various researchers have referred to this component as feedback-related negativity (FRN) [16] or feedback ERN (fERN) [17], we propose that this component be labeled as outcome-related negativity (ORN) for the following reasons: (1) the term outcome in ORN correctly denotes the quality (loss/gain) and quantity (large/small) of the outcome event that has a reinforcement value, (2) the term error in ERN and fERN may only be attributable for error-related paradigms, (3) the term MFN indicates the brain area of its origin (medial frontal area) but not the attributable function, and (4) the term feedback in FRN and fERN is a general term that may denote both error and outcome. Similarities and differences between these two negativities (i.e. ERN and ORN) are well described [18], [19].
Since the report by Gehring and Willoughby [15], who maintained that the negativity in the gambling paradigm was specific to the loss/gain dimension and not related to the error/correct dimension, several studies have examined the sensitivity and functional significance of the ORN in gambling tasks. For example, Nieuwenhuis et al. [19] used two experiments (emphasizing either loss/gain or error/correct dimension) and determined that the sensitivity of the negativity is dependent on which dimension is most salient. This phenomenon was termed context dependence. Functional magnetic resonance imaging (fMRI) of this feature elicited activations in prefrontal cortex, striatum, posterior cingulate, and inferior parietal lobule [20]. According to the context dependence hypothesis, the loss and gain (in the TCTO paradigms) were not based on the outcome of the chosen amount but rather on its ‘relative’ outcome compared to the other unchosen or alternative amount(s) [21]. For example, when 10 is chosen (between 10 and 50) and the Chosen Outcome Stimuli (COS) is +10 (a gain of 10), and the outcome of the unchosen Alternative Outcome Stimuli (AOS) is +50 (a gain of 50), the relative or ‘net’ outcome is −40 (a loss of 40); on the other hand, if the COS is −10 and the AOS is −50, then the net outcome is +40 (a gain of 40). This phenomenon of ‘net-loss’ and ‘net-gain’ was evident even for the neutral (no loss and no gain) COS which could elicit an ORN as large as that elicited by a negative COS, and thus the ORN was thought to reflect the binary evaluation of resultant good vs. bad outcomes [16], [17]. Yeung and Sanfey [22] reported that the ORN was found to be greater after losses than after gains but it was not significantly different between higher and lower amounts. Toyomaki and Murohashi [23] made an observation that the ORN elicited for the loss and neutral was larger than that of the gain condition, and the ORN was not affected by the magnitude of the bet. Interestingly, Yeung et al. [24] elicited ORNs in simple gambling tasks even when the participants made no active choices and made no overt actions. Further, Donkers et al. [25], using a simple slot-machine task, elicited the ORN for the subjective experience of loss and gain in the absence of active selection of choices. Masaki et al. [26] found that the interplay of preceding outcome and current choice influenced the ORN. They reported that the ORN amplitude was larger when the preceding outcome was gain and the current choice was 50 Yen (out of 50 and 10 Yen). Using a passive outcome paradigm, Potts et al. [27] found that the ORN trough was more negative (deeper) for the ‘unpredicted no-reward’ condition than the ‘predicted no-reward’ and ‘predicted reward’ conditions.
Apart from ORN, the P3 component of the ERP has also been studied to analyze whether this positivity is sensitive to valence (loss/gain) and amount (small or large). As previously discussed, we propose to term this positivity as outcome-related positivity (ORP). ORP can be defined as a large positivity occurring between 275 and 700 ms in response to outcome stimuli usually presented in gambling tasks. Very few studies have examined the ORP and ORN together. Yeung and Sanfey [22] reported that the ORP was sensitive to reward amount but insensitive to reward valence (with the ORN showing the opposite pattern), apart from the finding that the ORP (but not the ORN) showed sensitivity to the reward value of alternative outcomes. Apart from the finding that the peak-to-peak ORN amplitude of loss and neutral conditions were significantly larger than that of win conditions, Toyomaki and Murohashi [28] reported two important observations on ORP to imply that ORP was sensitive to both the quality (loss/gain) and quantity (larger/smaller) of the bet: (1) The ORP peak amplitudes of win conditions were larger than those of lose and neutral conditions, and (2) ORP peak amplitude of the 500 Yen condition was larger than those of 10 and 100 Yen conditions. Despite these prominent studies, the functional nature of ORP (in terms of quality and quantity of outcomes) is still unclear, maybe due to the paucity of studies, as the gambling paradigm is relatively new. On the other hand, a similar component in an error paradigm, called the error positivity (Pe), has been relatively well studied [29]. Pe is shown to reflect conscious recognition and motivational significance of the error in choice-reaction paradigms [29], [30]. On the other hand, the positivity in gambling paradigms (ORP) is considered to index the subjective evaluation of the magnitude of outcome in gambling tasks [22], [28]. However, the functional significance of ORP has not yet been validated by diverse gambling paradigms.
The nature, sensitivity and functional significance of outcome-related ERP components (specifically relating to the loss/gain dimension) have not yet been unequivocally established, perhaps because of the following reasons: (1) there has been no study that has used a gambling task to measure the loss/gain dimension without the confound of the error/correct dimension, (2) the sample size in general has been very small in reported studies, and (3) the gender effect in evaluative processing has not been analyzed in detail, although gender has considerable influence on behavioral and electrophysiological variables; e.g., ORP has been found to be larger in females than in males [31]. The present study has taken all of these issues into consideration.
Further, it is of interest to study aspects of impulsivity in the context of behavioral and ERP measures in a gambling paradigm, as it has already been shown in the error-related paradigms that the amplitude of the negative (Ne) and/or positive (Pe) component was sensitive to the level of impulsivity [13], [32], [33], [34]. Using a gambling task, a few studies have examined impulsivity related measures. For example, Gehring and Willoughby [15] showed the correspondence between risk-taking behavior and outcome processing in their finding on ORN (MFN) that the choices made after losses were riskier and were associated with greater loss-related activity than choices made after gains. Similarly, Yeung and Sanfey [22] reported that individual differences in the amplitude of the ORN correlated with individual differences in risk-taking behavior observed after monetary losses, whereas individual differences in ORP amplitude were related to behavioral adjustments observed in response to alternative or unchosen outcomes.
The main aim of the current study is to analyze ORN and ORP components of a single outcome gambling task (without the complexity and confound of the error/correct aspect) in the context of several key factors/dimensions, viz., loss/gain, 50/10, gender, impulsivity and behavioral measures. Our study therefore has been designed with the following objectives: (1) to analyze the ORN and ORP components in the context of valence (loss/gain) and amount (50/10) of outcomes, (2) to see the areas of neural activity (in terms of topography of surface potentials and current density) during different task conditions, (3) to analyze the behavioral and impulsivity variables that may be correlated with ORN and ORP, and (4) to evaluate gender differences, if any, in the ERP waveforms, topography, current density, and behavioral/impulsivity measures. Based on the previous findings and views, the hypotheses of the present study were four-fold: (1) the gain conditions will produce higher amplitude and shorter latency than the loss conditions in ORN and ORP components, (2) the larger amount will produce higher amplitude than the smaller amount in ORN and ORP components, (3) the higher the impulsivity related scores, the lower the amplitude and the shorter the latency of ORN and ORP components, (4) there will be gender differences while processing the quality and quantity of outcomes in ORN and ORP components, as well as in the impulsivity/behavioral measures. In the following sections, the terms ORN and ORP will, wherever appropriate, replace the terms N2 and P3 respectively. Further, the present study also examined the view that the loss and gain are mediated by separate and distinct brain regions, apart from the common areas associated with the reward circuitry [20]. As this study involved both surface potential and current density measures in each gender, it was expected to shed light on the understanding of gender differences with regard to the neurocognitive correlates of monetary loss and gain and of impulsivity.
Section snippets
Participants
The sample consisted of 50 healthy volunteers (25 males and 25 females) within the age range of 18–25 years. The participants were recruited through advertisements, and the study was conducted at SUNY Downstate Medical Center at Brooklyn, NY, USA. Individuals with hearing or visual impairment, severe medical (e.g., liver diseases, recent surgery, chronic pain conditions that may interfere with the performance of the task), neurological (e.g., dementia, delirium, head injury, degenerative
Behavioral data
Table 1 shows the comparison of behavioral measures across gender using t-tests. There was no significant difference between males and females in any of the variables after correcting for multiple testing using the Bonferroni method. However, before this correction, reaction time for the trials following −10 trials was significantly (p = 0.0293) longer in females. Females in general had longer reaction time than males for many variables, although they were not statistically significant.
The
Discussion
The main aim of the present study was to analyze ORN and ORP components of a single outcome gambling task (without the complexity and confound of the error/correct aspect) in the context of several key factors/dimensions, viz., valence, amount, gender, impulsivity and behavioral measures. Since our study has used a “single-outcome” gambling task (SOG), a novel paradigm, it is primarily exploratory in nature. While findings related to valence (loss/gain) and amount (50/10) dimensions (including
Acknowledgement
This study was supported by the National Institutes of Health (NIH) Grants #5 RO1 AA005524, AA02686 and AA008401 from the National Institute on Alcohol Abuse and Alcoholism (NIAAA). We are grateful for the valuable technical assistance of Carlene Haynes, Joyce Alonzia, Chamion Thomas, Tracy Crippen, Glenn Murawski, Eric Talbert, Patrick Harvey, Cindy Lipper, and Gabriel Wurzel.
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In memory of Dr. Henri Begleiter, we acknowledge with great admiration his seminal scientific contributions to the field. We are indebted to his charismatic leadership and luminous guidance. We are truly inspired by his visions to carry forward the work he fondly cherished.