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Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation.

ABSTRACT: Prolonged mesolimbic dopamine concentration changes have been detected during spatial navigation, but little is known about the conditions that engender this signaling profile or how it develops with learning. To address this, we monitored dopamine concentration changes in the nucleus accumbens core of rats throughout acquisition and performance of an instrumental action sequence task. Prolonged dopamine concentration changes were detected that ramped up as rats executed each action sequence and declined after earned reward collection. With learning, dopamine concentration began to rise increasingly earlier in the execution of the sequence and ultimately backpropagated away from stereotyped sequence actions, becoming only transiently elevated by the most distal and unexpected reward predictor. Action sequence-related dopamine signaling was reactivated in well-trained rats if they became disengaged in the task and in response to an unexpected change in the value, but not identity of the earned reward. Throughout training and test, dopamine signaling correlated with sequence performance. These results suggest that action sequences can engender a prolonged mode of dopamine signaling in the nucleus accumbens core and that such signaling relates to elements of the motivation underlying sequence execution and is dynamic with learning, overtraining and violations in reward expectation.

SUBMITTER: Collins AL

PROVIDER: S-EPMC4751524 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation.

Collins Anne L AL Greenfield Venuz Y VY Bye Jeffrey K JK Linker Kay E KE Wang Alice S AS Wassum Kate M KM

Scientific reports 20160212

Prolonged mesolimbic dopamine concentration changes have been detected during spatial navigation, but little is known about the conditions that engender this signaling profile or how it develops with learning. To address this, we monitored dopamine concentration changes in the nucleus accumbens core of rats throughout acquisition and performance of an instrumental action sequence task. Prolonged dopamine concentration changes were detected that ramped up as rats executed each action sequence and ...[more]

PMID: 26869075

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Project description:The brain is subjected to multi-modal sensory information in an environment governed by statistical dependencies. Mismatch responses (MMRs), classically recorded with EEG, have provided valuable insights into the brain's processing of regularities and the generation of corresponding sensory predictions. Only few studies allow for comparisons of MMRs across multiple modalities in a simultaneous sensory stream and their corresponding cross-modal context sensitivity remains unknown. Here, we used a tri-modal version of the roving stimulus paradigm in fMRI to elicit MMRs in the auditory, somatosensory and visual modality. Participants (N = 29) were simultaneously presented with sequences of low and high intensity stimuli in each of the three senses while actively observing the tri-modal input stream and occasionally reporting the intensity of the previous stimulus in a prompted modality. The sequences were based on a probabilistic model, defining transition probabilities such that, for each modality, stimuli were more likely to repeat (p = .825) than change (p = .175) and stimulus intensities were equiprobable (p = .5). Moreover, each transition was conditional on the configuration of the other two modalities comprising global (cross-modal) predictive properties of the sequences. We identified a shared mismatch network of modality general inferior frontal and temporo-parietal areas as well as sensory areas, where the connectivity (psychophysiological interaction) between these regions was modulated during mismatch processing. Further, we found deviant responses within the network to be modulated by local stimulus repetition, which suggests highly comparable processing of expectation violation across modalities. Moreover, hierarchically higher regions of the mismatch network in the temporo-parietal area around the intraparietal sulcus were identified to signal cross-modal expectation violation. With the consistency of MMRs across audition, somatosensation and vision, our study provides insights into a shared cortical network of uni- and multi-modal expectation violation in response to sequence regularities.

Project description:Modifying patients' expectations by exposing them to expectation violation situations (thus maximizing the difference between the expected and the actual situational outcome) is proposed to be a crucial mechanism for therapeutic success for a variety of different mental disorders. However, clinical observations suggest that patients often maintain their expectations regardless of experiences contradicting their expectations. It remains unclear which information processing mechanisms lead to modification or persistence of patients' expectations. Insight in the processing could be provided by Neuroimaging studies investigating prediction error (PE, i.e., neuronal reactions to non-expected stimuli). Two methods are often used to investigate the PE: (1) paradigms, in which participants passively observe PEs ("passive" paradigms) and (2) paradigms, which encourage a behavioral adaptation following a PE ("active" paradigms). These paradigms are similar to the methods used to induce expectation violations in clinical settings: (1) the confrontation with an expectation violation situation and (2) an enhanced confrontation in which the patient actively challenges his expectation. We used this similarity to gain insight in the different neuronal processing of the two PE paradigms. We performed a meta-analysis contrasting neuronal activity of PE paradigms encouraging a behavioral adaptation following a PE and paradigms enforcing passiveness following a PE. We found more neuronal activity in the striatum, the insula and the fusiform gyrus in studies encouraging behavioral adaptation following a PE. Due to the involvement of reward assessment and avoidance learning associated with the striatum and the insula we propose that the deliberate execution of action alternatives following a PE is associated with the integration of new information into previously existing expectations, therefore leading to an expectation change. While further research is needed to directly assess expectations of participants, this study provides new insights into the information processing mechanisms following an expectation violation.

Dataset Information

Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation.

Publications

Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation.

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