Abstract:We enjoy a sophisticated understanding of how animals learn to predict appetitive outcomes and direct their behaviour accordingly. This encompasses well-defined learning algorithms and details of how these might be implemented in the brain. Dopamine has played an important part in this unfolding story, appearing to embody a learning signal for predicting rewards and stamping in useful actions, while also being a modulator of behavioural vigour. By contrast, although choosing correct actions and executing them … Show more
“…We found that phasic DA release in NAcC at the WS reliably predicted successful avoidance [12]. This release pattern is analogous to that seen with appetitive cues and is thus hypothesized to reflect an animal’s expectation that shock is avoidable (safety is attainable) [13, 14], driving active avoidance. Conversely, DA release was decreased at the WS prior to escape [8].…”
Phasic dopamine (DA) release accompanies approach toward appetitive cues. However, a role for DA in the active avoidance of negative events remains undetermined. Warning signals informing footshock avoidance are associated with accumbal DA release, whereas depression of DA is observed with unavoidable footshock. Here, we reveal a causal role of phasic DA in active avoidance learning; specifically, optogenetic activation of DA neurons facilitates avoidance, whereas optical inhibition of these cells attenuates it. Furthermore, stimulation of DA neurons during presentation of a fear-conditioned cue accelerates the extinction of a passive defensive behavior (i.e., freezing). Dopaminergic control of avoidance requires endocannabinoids (eCBs), as perturbing eCB signaling in the midbrain disrupts avoidance, which is rescued by optical stimulation of DA neurons. Interestingly, once the avoidance task is learned, neither DA nor eCB manipulations affect performance, suggesting that once acquisition occurs, expression of this behavior is subserved by other anatomical frameworks. Our findings establish an instrumental role for DA release in learning active responses to aversive stimuli and its control by eCB signaling.
“…We found that phasic DA release in NAcC at the WS reliably predicted successful avoidance [12]. This release pattern is analogous to that seen with appetitive cues and is thus hypothesized to reflect an animal’s expectation that shock is avoidable (safety is attainable) [13, 14], driving active avoidance. Conversely, DA release was decreased at the WS prior to escape [8].…”
Phasic dopamine (DA) release accompanies approach toward appetitive cues. However, a role for DA in the active avoidance of negative events remains undetermined. Warning signals informing footshock avoidance are associated with accumbal DA release, whereas depression of DA is observed with unavoidable footshock. Here, we reveal a causal role of phasic DA in active avoidance learning; specifically, optogenetic activation of DA neurons facilitates avoidance, whereas optical inhibition of these cells attenuates it. Furthermore, stimulation of DA neurons during presentation of a fear-conditioned cue accelerates the extinction of a passive defensive behavior (i.e., freezing). Dopaminergic control of avoidance requires endocannabinoids (eCBs), as perturbing eCB signaling in the midbrain disrupts avoidance, which is rescued by optical stimulation of DA neurons. Interestingly, once the avoidance task is learned, neither DA nor eCB manipulations affect performance, suggesting that once acquisition occurs, expression of this behavior is subserved by other anatomical frameworks. Our findings establish an instrumental role for DA release in learning active responses to aversive stimuli and its control by eCB signaling.
“…Current views of striatal dopamine function (Collins and Frank, 2015; 2014; Frank, 2006; Frank, 2005; Lloyd and Dayan, 2016) suggest that the striatal architecture is well suited to implement the Pavlovian asymmetry in behavioural activation. Appetitive (aversive) conditioned cues elicit peaks (dips) in mesolimbic dopamine release in the striatum (Cohen et al, 2012; Day et al, 2007; Matsumoto and Hikosaka, 2009; Tobler et al, 2005).…”
Section: Discussionmentioning
confidence: 99%
“…Enhanced dopamine increases appetitive PIT (Wyvell and Berridge, 2000), while appetitive PIT is lowered when striatal dopamine is reduced (Dickinson et al, 2000; Hebart and Gläscher, 2015; Lex and Hauber, 2008). Striatal dopamine has also been linked to controlling aversively motivated behaviour (Faure et al, 2008; Lloyd and Dayan, 2016). Together, these results show that appetitive cues promote activation and aversive cues promote inhibition in a Pavlovian manner, mediated by the dopamine system.10.7554/eLife.22169.003Figure 1.Distinct mechanisms by which motivational valence may bias behavioural activation.( A ) Pavlovian response bias: appetitive cues (green edge) elicit generalized behavioural activation (‘Go’), whereas aversive cues (red edge) elicit behavioural inhibition (‘NoGo’).…”
Catecholamines modulate the impact of motivational cues on action. Such motivational biases have been proposed to reflect cue-based, ‘Pavlovian’ effects. Here, we assess whether motivational biases may also arise from asymmetrical instrumental learning of active and passive responses following reward and punishment outcomes. We present a novel paradigm, allowing us to disentangle the impact of reward and punishment on instrumental learning from Pavlovian response biasing. Computational analyses showed that motivational biases reflect both Pavlovian and instrumental effects: reward and punishment cues promoted generalized (in)action in a Pavlovian manner, whereas outcomes enhanced instrumental (un)learning of chosen actions. These cue- and outcome-based biases were altered independently by the catecholamine enhancer melthylphenidate. Methylphenidate’s effect varied across individuals with a putative proxy of baseline dopamine synthesis capacity, working memory span. Our study uncovers two distinct mechanisms by which motivation impacts behaviour, and helps refine current models of catecholaminergic modulation of motivated action.DOI:
http://dx.doi.org/10.7554/eLife.22169.001
“…Among animals of a particular species, certain avoidance behaviors are instinctive punishment responses and can be transferred very easily from US to CS; others have to be learned based on their potential to facilitate escape [for a review, see Ref. (160)]. Though analogous to the learning of appetitive behaviors to obtain rewards, avoidance learning poses an additional theoretical challenge because reinforcement in this case depends on non-occurrence of an aversive event.…”
Section: Trait Anxiety: Targets For Computational Studiesmentioning
confidence: 99%
“…Working independently or in combination over a long period of time, these two mechanisms would have the overall effect of reducing an animal’s exploration of fear-associated regions of state space by making avoidance more likely (160). This would prevent the animal from learning that its fears were exaggerated.…”
Section: Trait Anxiety: Targets For Computational Studiesmentioning
Computational methods are increasingly being applied to the study of psychiatric disorders. Often, this involves fitting models to the behavior of individuals with subclinical character traits that are known vulnerability factors for the development of psychiatric conditions. Anxiety disorders can be examined with reference to the behavior of individuals high in “trait” anxiety, which is a known vulnerability factor for the development of anxiety and mood disorders. However, it is not clear how this self-report measure relates to neural and behavioral processes captured by computational models. This paper reviews emerging computational approaches to the study of trait anxiety, specifying how interacting processes susceptible to analysis using computational models could drive a tendency to experience frequent anxious states and promote vulnerability to the development of clinical disorders. Existing computational studies are described in the light of this perspective and appropriate targets for future studies are discussed.
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