Common and Distinct Functional Brain Networks for Intuitive and Deliberate Decision Making

Reinforcement learning studies in rodents and primates demonstrate that goal-directed and habitual choice behaviors are mediated through different fronto-striatal systems, but the evidence is less clear in humans. In this study, functional magnetic resonance imaging (fMRI) data were collected whilst participants ( n = 20) performed a conditional associative learning task in which blocks of novel conditional stimuli (CS) required a deliberate choice, and blocks of familiar CS required an intuitive choice. Using standard subtraction analysis for fMRI event-related designs, activation shifted from the dorso-fronto-parietal network, which involves dorsolateral prefrontal cortex (DLPFC) for deliberate choice of novel CS, to ventro-medial frontal (VMPFC) and anterior cingulate cortex for intuitive choice of familiar CS. Supporting this finding, psycho-physiological interaction (PPI) analysis, using the peak active areas within the PFC for novel and familiar CS as seed regions, showed functional coupling between caudate and DLPFC when processing novel CS and VMPFC when processing familiar CS. These findings demonstrate separable systems for deliberate and intuitive processing, which is in keeping with rodent and primate reinforcement learning studies, although in humans they operate in a dynamic, possibly synergistic, manner particularly at the level of the striatum.Peer reviewedFinal Published versio

Neural Correlates of Instrumental Contingency Learning: Differential Effects of Action–Reward Conjunction and Disjunction

Contingency theories of goal-directed action propose that experienced disjunctions between an action and its specific consequences, as well as conjunctions between these events, contribute to encoding the action–outcome association. Although considerable behavioral research in rats and humans has provided evidence for this proposal, relatively little is known about the neural processes that contribute to the two components of the contingency calculation. Specifically, while recent findings suggest that the influence of action–outcome conjunctions on goal-directed learning is mediated by a circuit involving ventromedial prefrontal, medial orbitofrontal cortex, and dorsomedial striatum, the neural processes that mediate the influence of experienced disjunctions between these events are unknown. Here we show differential responses to probabilities of conjunctive and disjunctive reward deliveries in the ventromedial prefrontal cortex, the dorsomedial striatum, and the inferior frontal gyrus. Importantly, activity in the inferior parietal lobule and the left middle frontal gyrus varied with a formal integration of the two reward probabilities, ΔP, as did response rates and explicit judgments of the causal efficacy of the action

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

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

Electrocortical components of anticipation and consumption in a monetary incentive delay task

In order to improve our understanding of the components that reflect functionally important processes during reward anticipation and consumption, we used principle components analyses (PCA) to separate and quantify averaged ERP data obtained from each stage of a modified monetary incentive delay (MID) task. Although a small number of recent ERP studies have reported that reward and loss cues potentiate ERPs during anticipation, action preparation, and consummatory stages of reward processing, these findings are inconsistent due to temporal and spatial overlap between the relevant electrophysiological components. Our results show three components following cue presentation are sensitive to incentive cues (N1, P3a, P3b). In contrast to previous research, reward‐related enhancement occurred only in the P3b, with earlier components more sensitive to break‐even and loss cues. During feedback anticipation, we observed a lateralized centroparietal negativity that was sensitive to response hand but not cue type. We also show that use of PCA on ERPs reflecting reward consumption successfully separates the reward positivity from the independently modulated feedback‐P3. Last, we observe for the first time a new reward consumption component: a late negativity distributed over the left frontal pole. This component appears to be sensitive to response hand, especially in the context of monetary gain. These results illustrate that the time course and sensitivities of electrophysiological activity that follows incentive cues do not follow a simple heuristic in which reward incentive cues produce enhanced activity at all stages and substages

Inferring action-dependent outcome representations depends on anterior but not posterior medial orbitofrontal cortex

© 2018 Elsevier Inc. Although studies examining orbitofrontal cortex (OFC) often treat it as though it were functionally homogeneous, recent evidence has questioned this assumption. Not only are the various subregions of OFC (lateral, ventral, and medial) hetereogeneous, but there is further evidence of heterogeneity within those subregions. For example, several studies in both humans and monkeys have revealed a functional subdivision along the anterior-posterior gradient of the medial OFC (mOFC). Given our previous findings suggesting that, in rats, the mOFC is responsible for inferring the likelihood of unobservable action outcomes (Bradfield, Dezfouli, van Holstein, Chieng, & Balleine, 2015), and given the anterior nature of the placements of our prior manipulations, we decided to assess whether the rat mOFC also differs in connection and function along its anteroposterior axis. We first used retrograde tracing to compare the density of efferents from mOFC to several structures known to contribute to goal-directed action: the mediodorsal thalamus, basolateral amygdala, posterior dorsomedial striatum, nucleus accumbens core and ventral tegmental area. We then compared the functional effects of anterior versus posterior mOFC excitotoxic lesions on tests of Pavlovian-instrumental transfer, instrumental outcome devaluation and outcome-specific reinstatement. We found evidence that the anterior mOFC had greater connectivity with the accumbens core and greater functional involvement in goal-directed action than the posterior mOFC. Consistent with previous findings across species, therefore, these results suggest that the anterior and posterior mOFC of the rat are indeed functionally distinct, and that it is the anterior mOFC that is particularly critical for inferring unobservable action outcomes

Prefrontal corticostriatal disconnection blocks the acquisition of goal-directed action

© 2018 the authors. The acquisition of goal-directed action requires encoding of the association between an action and its specific consequences or outcome. At a neural level, this encoding has been hypothesized to involve a prefrontal corticostriatal circuit involving the projection from the prelimbic cortex (PL) to the posterior dorsomedial striatum (pDMS); however, no direct evidence for this claim has been reported. In a series of experiments, we performed functional disconnection of this pathway using targeted lesions of the anterior corpus callosum to disrupt contralateral corticostriatal projections with asymmetrical lesions of the PL and/orpDMSto block plasticity in this circuit in rats. We first demonstrated that unilaterally blocking the PL input to the pDMS prevented the phosphorylation of extracellular signal-related kinase/mitogen activated protein kinase (pERK/pMAPK) induced by instrumental training. Next, we used a full bilateral disconnection of the PL from the pDMS and assessed goal-directed action using an outcome-devaluation test. Importantly, we found evidence that rats maintaining an ipsilateral and/or contralateral connection between thePLand thepDMSwere able to acquire goal-directed actions. In contrast, bilateral PL–pDMS disconnection abolished the acquisition of goal-directed actions. Finally, we used a temporary pharmacological disconnection to disrupt PL inputs to thepDMSby infusing theNMDAantagonist DL-2-amino-5-phosphonopentanoic acid into thepDMSduring instrumental training and found that this manipulation also disrupted goal-directed learning. These results establish that, in rats, the acquisition of new goal-directed actions depends on a prefrontal-corticostriatal circuit involving a connection between the PL and the pDMS

An anatomy of change : profiling cohort difference in beliefs and attitudes among Anglicans in England

Conservatism in theological belief, moral values and attitude toward ecclesiastical practices was measured in a sample of 5967 ordained and lay Anglicans in the Church of England. Average scores were compared between those who classed themselves as Anglo-catholic, broad church or evangelical, and by six different age cohorts. Overall, most measures of conservatism showed decline among more recent cohorts, but there were marked differences between traditions. Younger evangelicals showed little or no decline in theological or moral conservatism, and, in the case of Bible beliefs, were more conservative than their older counterparts. In ecclesiastical variables, however, Anglo-catholics were often more conservative and younger evangelicals showed less conservatism than other traditions or older evangelicals. The findings suggest that the divide between traditions is increasing among younger generations mainly because those in Anglo-catholic and broad-church traditions are becoming more liberal on theological or moral matters, whereas evangelicals are maintaining traditional conservative views of theology and morality but becoming less traditional in matters ecclesiastical

Plasticity in striatopallidal projection neurons mediates the acquisition of habitual actions

In instrumental conditioning, newly acquired actions are generally goal-directed and are mediated by the relationship between the action and its consequences or outcome. With continued training, however, the performance of such actions can become automatic, reflexive or habitual and under the control of antecedent stimuli rather than their consequences. Recent evidence suggests that habit learning is mediated by plasticity in the dorsolateral striatum (DLS). To date, however, no direct evidence of learning-related plasticity associated with overtraining has been reported in this region, nor is it known whether, or which, specific cell types are involved in this learning process. The striatum is primarily composed of two classes of spiny projection neurons, the striatonigral and striatopallidal spiny projection neurons, which express dopamine D1 and D2 receptors, and control direct and indirect pathways, respectively. Here we found evidence of a post-synaptic depression in DLS striatopallidal projecting neurons in the indirect pathway during habit learning in mice. Moreover, this training-induced depression occluded post-synaptic depression induced by co-activation of D2 receptors and transient receptor potential vanilloid 1 (TRPV1) channels, implying that this pathway is involved in habit learning. This hypothesis was further tested by disrupting this signal pathway by knocking out TRPV1 channels, resulting in compromised habit learning. Our findings suggest that post-synaptic plasticity at D2 neurons in the DLS mediates habit learning and, by implicating an interaction between the D2 receptor and TRPV1 channel activity, provide a potential drug target for influencing habitual action control.NHMRC grants: 1045964 & 108925

A specific role for posterior dorsolateral striatum in human habit learning

Habits are characterized by an insensitivity to their consequences and, as such, can be distinguished from goal-directed actions. The neural basis of the development of demonstrably outcome-insensitive habitual actions in humans has not been previously characterized. In this experiment, we show that extensive training on a free-operant task reduces the sensitivity of participants' behavior to a reduction in outcome value. Analysis of functional magnetic resonance imaging data acquired during training revealed a significant increase in task-related cue sensitivity in a right posterior putamen–globus pallidus region as training progressed. These results provide evidence for a shift from goal-directed to habit-based control of instrumental actions in humans, and suggest that cue-driven activation in a specific region of dorsolateral posterior putamen may contribute to the habitual control of behavior in humans