The Neural Mechanisms Underlying the Influence of Pavlovian Cues on Human Decision Making

Computation and Neural Systems, California Institute of Technology, Pasadena, California 91125, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 06/2008; 28(22):5861-6. DOI: 10.1523/JNEUROSCI.0897-08.2008
Source: PubMed


In outcome-specific transfer, pavlovian cues that are predictive of specific outcomes bias action choice toward actions associated with those outcomes. This transfer occurs despite no explicit training of the instrumental actions in the presence of pavlovian cues. The neural substrates of this effect in humans are unknown. To address this, we scanned 23 human subjects with functional magnetic resonance imaging while they made choices between different liquid food rewards in the presence of pavlovian cues previously associated with one of these outcomes. We found behavioral evidence of outcome-specific transfer effects in our subjects, as well as differential blood oxygenation level-dependent activity in a region of ventrolateral putamen when subjects chose, respectively, actions consistent and inconsistent with the pavlovian-predicted outcome. Our results suggest that choosing an action incompatible with a pavlovian-predicted outcome might require the inhibition of feasible but nonselected action-outcome associations. The results of this study are relevant for understanding how marketing actions can affect consumer choice behavior as well as for how environmental cues can influence drug-seeking behavior in addiction.

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    • "In humans, Pavlovian influences are evidenced by a series of experiments (Crockett et al., 2009; Guitart-Masip et al., 2011, 2012, 2014; Cavanagh et al., 2013) crossing motivational valence (appetitive vs. aversive) and action (behavioral activation vs. behavioral inhibition) showing that reward potentiates behavioral activation, while punishment potentiates behavioral inhibition (see also, Carver and White, 1994; Gray and McNaughton, 2000, where close reward-activation and punishment-inhibition couplings have been suggested). Similar Pavlovian response tendencies have been studied extensively using Pavlovian-to-instrumental transfer paradigms in animals, as well as humans, where reward- or punishment-predictive stimuli modulate instrumental responses (Estes and Skinner, 1941; Estes, 1948; Di Giusto et al., 1974; Lovibond, 1983; Dickinson and Balleine, 1994; Bray et al., 2008; Talmi et al., 2008; Declercq and De Houwer, 2009; Trick et al., 2011; Prévost et al., 2012; Geurts et al., 2013; Lewis et al., 2013; Lovibond et al., 2013). Although it has been shown before that basic learning mechanisms may be relevant to understanding human social interactions (Olsson et al., 2005), the hypothesis that Pavlovian-like response tendencies account for emotional biasing of action selection by emotional faces has never been tested. "
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    ABSTRACT: Instrumental decision making has long been argued to be vulnerable to emotional responses. Literature on multiple decision making systems suggests that this emotional biasing might reflect effects of a system that regulates innately specified, evolutionarily preprogrammed responses. To test this hypothesis directly, we investigated whether effects of emotional faces on instrumental action can be predicted by effects of emotional faces on bodily freezing, an innately specified response to aversive relative to appetitive cues. We tested 43 women using a novel emotional decision making task combined with posturography, which involves a force platform to detect small oscillations of the body to accurately quantify postural control in upright stance. On the platform, participants learned whole body approach-avoidance actions based on monetary feedback, while being primed by emotional faces (angry/happy). Our data evidence an emotional biasing of instrumental action. Thus, angry relative to happy faces slowed instrumental approach relative to avoidance responses. Critically, individual differences in this emotional biasing effect were predicted by individual differences in bodily freezing. This result suggests that emotional biasing of instrumental action involves interaction with a system that controls innately specified responses. Furthermore, our findings help bridge (animal and human) decision making and emotion research to advance our mechanistic understanding of decision making anomalies in daily encounters as well as in a wide range of psychopathology.
    Frontiers in Behavioral Neuroscience 07/2014; 8:237. DOI:10.3389/fnbeh.2014.00237 · 3.27 Impact Factor
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    • "In rodents, stress has been found not to behaviorally impair Pavlovian conditioning itself, but rather to lead to deficiencies in Pavlovian-to-instrumental transfer (Morgado et al., 2012)—a measure of the influence of Pavlovian cues on instrumental behavior (for review, see Dickinson and Balleine, 1994). Pavlovian-to instrumental transfer has been associated with increased activity in the striatum, particularly the putamen in humans (Bray et al., 2008; Prevost et al., 2012), and the effect of acute stress on this phenomenon might further elucidate the manner in which stress impacts striatal activity during Pavlovian conditioning. "
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    ABSTRACT: Pavlovian conditioning involves the association of an inherently neutral stimulus with an appetitive or aversive outcome, such that the neutral stimulus itself acquires reinforcing properties. Across species, this type of learning has been shown to involve subcortical brain regions such as the striatum and the amygdala. It is less clear, however, how the neural circuitry involved in the acquisition of Pavlovian contingencies in humans, particularly in the striatum, is affected by acute stress. In the current study, we investigate the effect of acute stress exposure on Pavlovian conditioning using monetary reinforcers. Participants underwent a partial reinforcement conditioning procedure in which neutral stimuli were paired with high and low magnitude monetary gains and losses. A between-subjects design was used, such that half of the participants were exposed to cold stress while the remaining participants were exposed to a no stress control procedure. Cortisol measurements and subjective ratings were used as measures of stress. We observed an interaction between stress, valence, and magnitude in the ventral striatum, with the peak in the putamen. More specifically, the stress group exhibited an increased sensitivity to magnitude in the gain domain. This effect was driven by those participants who experienced a larger increase in circulating cortisol levels in response to the stress manipulation. Taken together, these results suggest that acute stress can lead to individual differences in circulating cortisol levels which influence the striatum during Pavlovian conditioning with monetary reinforcers.
    Frontiers in Behavioral Neuroscience 05/2014; 8:179. DOI:10.3389/fnbeh.2014.00179 · 3.27 Impact Factor
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    • "Previous animal and human studies have characterised the patterns of brain activation that underlie PIT effects produced by natural rewards, and have consistently revealed that the striatum, amygdala, orbitofrontal cortex and mediodorsal thalamus are involved [13]. Other studies have used electroencephalography (EEG) to examine electrophysiological indices of drug cue reactivity and these studies suggest that event-related potentials (ERPs) can provide a sensitive measure of brain activity when registering the motivational salience of drug-related pictorial cues [14]. "
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    ABSTRACT: Pavlovian to Instrumental Transfer (PIT) refers to the behavioral phenomenon of increased instrumental responding for a reinforcer when in the presence of Pavlovian conditioned stimuli that were separately paired with that reinforcer. PIT effects may play an important role in substance use disorders, but little is known about the brain mechanisms that underlie these effects in alcohol consumers. We report behavioral and electroencephalographic (EEG) data from a group of social drinkers (n = 31) who performed a PIT task in which they chose between two instrumental responses in pursuit of beer and chocolate reinforcers while their EEG reactivity to beer, chocolate and neutral pictorial cues was recorded. We examined two markers of the motivational salience of the pictures: the P300 and slow wave event-related potentials (ERPs). Results demonstrated a behavioral PIT effect: responding for beer was increased when a beer picture was presented. Analyses of ERP amplitudes demonstrated significantly larger slow potentials evoked by beer cues at various electrode clusters. Contrary to hypotheses, there were no significant correlations between behavioral PIT effects, electrophysiological reactivity to the cues, and individual differences in drinking behaviour. Our findings are the first to demonstrate a PIT effect for beer, accompanied by increased slow potentials in response to beer cues, in social drinkers. The lack of relationship between behavioral and EEG measures, and between these measures and individual differences in drinking behaviour may be attributed to methodological features of the PIT task and to characteristics of our sample.
    PLoS ONE 04/2014; 9(4):e94605. DOI:10.1371/journal.pone.0094605 · 3.23 Impact Factor
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