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Esber, G. R.

Publications and source records attributed to Esber, G. R..

6 recordsLinked to original sources

Rewarding Value or Prediction Error: Settling the debate over the role of dopamine in reward learning

The discovery that DA transients can be mapped onto the reward prediction errors in temporal difference models is a pinnacle achievement of neuroscience. Yet, there is abundant evidence that DA activity reinforces actions, suggesting it serves as an intrinsically rewarding event. These two possibilities are so conceptually intertwined that it is not surprising that they have been so far experimentally conflated. Here, using computational modeling, behavioural blocking and optogenetics, we show that stimulating VTA DA neurons promotes learning even when a natural reward and DA stimulation are held constant across the learning phases of blocking. These findings provide strong evidence in favour of the prediction error hypothesis rather than encoding the rewarding value of appetitive events.

neuroscience↗

A critical contribution of a sparse neuronal ensemble in the amygdala central nucleus to extinction

Adaptive behaviour critically depends on the delicate and dynamic balance between acquisition and extinction memories. Disruption of this balance, particularly when the extinction memory loses control over behaviour, is the root of treatment failure of maladaptive behaviours such as substance abuse or anxiety disorders. Understanding this balance requires a better understanding of the underlying neurobiology and its contribution to behavioural regulation. Here, we used Daun02 in Fos-lacZ transgenic rats to delete extinction-recruited neuronal ensembles in BLA and CN and examine their contribution to behaviour in an appetitive Pavlovian task. Deletion of extinction-activated ensembles in CN but not BLA impaired the retrieval of extinction and increased activity in the BLA. The disruptive effect of deleting these CN ensembles was enduring as it hindered further extinction learning, and promoted greater levels of behavioural restoration across opposing levels of the response scale seen in spontaneous recovery and reinstatement. Our data indicate that the initial extinction-recruited CN ensemble is critical to the acquisition-extinction balance, and that greater behavioural restoration does not mean weaker extinction contribution. These findings provide a novel avenue for thinking about the neural mechanisms of extinction and in developing treatments for cue-triggered appetitive behaviours.

neuroscience↗

Surprise-induced enhancements in the associability of Pavlovian cues facilitate learning across behavior systems

Surprising violations of outcome expectancies have long been known to enhance the associability of Pavlovian cues; that is, the rate at which the cue enters into further associations. The adaptive value of such enhancements resides in promoting new learning in the face of uncertainty. However, it is unclear whether associability enhancements reflect increased associative plasticity within a particular behavior system, or whether they can facilitate learning between a cue and any arbitrary outcome, as suggested by attentional models of conditioning. Here, we show evidence consistent with the latter hypothesis. Violating the outcome expectancies generated by a cue in an appetitive setting (feeding behavior system) facilitated subsequent learning about the cue in an aversive setting (defense behavior system). In addition to shedding light on the nature of associability enhancements, our findings offer the neuroscientist a behavioral tool to dissociate their neural substrates from those of other, behavior system- or valence-specific changes. Moreover, our results present an opportunity to utilize associability enhancements to the advantage of counterconditioning procedures in therapeutic contexts.

animal behavior and cognition↗

Agency rescues competition for credit assignment among predictive cues from adverse learning conditions

A fundamental assumption of learning theories is that the credit assigned to predictive cues is not simply determined by their probability of reinforcement, but by their ability to compete with other cues present during learning. This assumption has guided behavioral and neural science research for decades, and tremendous empirical and theoretical advances have been made identifying the mechanisms of cue competition. However, when learning conditions are not optimal (e.g., when training is massed), credit assignment is no longer competitive. This is a catastrophic failure of the learning system that exposes the individuals vulnerability to form spurious associations in the real world. Here, we uncover that cue competition can be rescued when conditions are suboptimal provided that the individual has agency over the learning experience. Our findings reveal a new connection between agency over learning and credit assignment to cues, and open new avenues of investigation into the underlying mechanisms.

animal behavior and cognition↗

A self-initiated cue-reward learning procedure for neural recording in rodents

BackgroundSingle-unit recording in Pavlovian conditioning tasks requires the use of within-subject designs as well as sampling a considerable number of trials per trial type and session, which increases the total trial count. Pavlovian conditioning, on the other hand, requires a long average intertrial interval (ITI) relative to cue duration for cue-specific learning to occur. These requirements combined can make the session duration unfeasibly long. New MethodTo circumvent this issue, we developed a self-initiated variant of the Pavlovian magazine-approach procedure in rodents. Unlike the standard procedure, where the animals passively receive the trials, the self-initiated procedure grants animals agency to self-administer and self-pace trials from a predetermined, pseudorandomized list. Critically, whereas in the standard procedure the typical ITI is in the order of minutes, our procedure uses a much shorter ITI (10 s). ResultsDespite such a short ITI, discrimination learning in the self-initiated procedure is comparable to that observed in the standard procedure with a typical ITI, and superior to that observed in the standard procedure with an equally short ITI. Comparison with Existing Method(s)The self-initiated procedure permits delivering 100 trials in a [~]1-h session, almost doubling the number of trials safely attainable over that period with the standard procedure. ConclusionsThe self-initiated procedure enhances the collection of neural correlates of cue-reward learning while producing good discrimination performance. Other advantages for neural recording studies include ensuring that at the start of each trial the animal is engaged, attentive and in the same location within the conditioning chamber.

neuroscience↗

Different forms of fear extinction are supported by distinct cortical substrates

Understanding how learned fear can be reduced is at the heart of treatments for anxiety disorders. Tremendous progress has been made in this regard through extinction training in which an expected aversive outcome is omitted. However, current progress almost entirely rests on this single paradigm, resulting in a very specialized knowledgebase at the behavioural and neural level of analysis. Here, we used a paradigm-independent approach to show that different methods that lead to reduction in learned fear are dissociated in the cortex. We report that the infralimbic cortex has a very specific role in fear reduction that depends on the omission of aversive events but not on overexpectation. The orbitofrontal cortex, a structure generally overlooked in fear, is critical for downregulating fear when fear is inflated or overexpected, but not when an aversive event is omitted.

neuroscience↗