scholarly journals A VTA GABAergic computational model of dissociated reward prediction error computation in classical conditioning

2020 ◽  
Author(s):  
Pramod Kaushik ◽  
Jérémie Naudé ◽  
Surampudi Bapi Raju ◽  
Frédéric Alexandre

AbstractClassical Conditioning is a fundamental learning mechanism where the Ventral Striatum is generally thought to be the source of inhibition to Ventral Tegmental Area (VTA) Dopamine neurons when a reward is expected. However, recent evidences point to a new candidate in VTA GABA encoding expectation for computing the reward prediction error in the VTA. In this system-level computational model, the VTA GABA signal is hypothesised to be a combination of magnitude and timing computed in the Peduncolopontine and Ventral Striatum respectively. This dissociation enables the model to explain recent results wherein Ventral Striatum lesions affected the temporal expectation of the reward but the magnitude of the reward was intact. This model also exhibits other features in classical conditioning namely, progressively decreasing firing for early rewards closer to the actual reward, twin peaks of VTA dopamine during training and cancellation of US dopamine after training.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
William Menegas ◽  
Benedicte M Babayan ◽  
Naoshige Uchida ◽  
Mitsuko Watabe-Uchida

Dopamine neurons are thought to encode novelty in addition to reward prediction error (the discrepancy between actual and predicted values). In this study, we compared dopamine activity across the striatum using fiber fluorometry in mice. During classical conditioning, we observed opposite dynamics in dopamine axon signals in the ventral striatum (‘VS dopamine’) and the posterior tail of the striatum (‘TS dopamine’). TS dopamine showed strong excitation to novel cues, whereas VS dopamine showed no responses to novel cues until they had been paired with a reward. TS dopamine cue responses decreased over time, depending on what the cue predicted. Additionally, TS dopamine showed excitation to several types of stimuli including rewarding, aversive, and neutral stimuli whereas VS dopamine showed excitation only to reward or reward-predicting cues. Together, these results demonstrate that dopamine novelty signals are localized in TS along with general salience signals, while VS dopamine reliably encodes reward prediction error.



2007 ◽  
Vol 97 (4) ◽  
pp. 3036-3045 ◽  
Author(s):  
Signe Bray ◽  
John O'Doherty

Attractive faces can be considered to be a form of visual reward. Previous imaging studies have reported activity in reward structures including orbitofrontal cortex and nucleus accumbens during presentation of attractive faces. Given that these stimuli appear to act as rewards, we set out to explore whether it was possible to establish conditioning in human subjects by pairing presentation of arbitrary affectively neutral stimuli with subsequent presentation of attractive and unattractive faces. Furthermore, we scanned human subjects with functional magnetic resonance imaging (fMRI) while they underwent this conditioning procedure to determine whether a reward-prediction error signal is engaged during learning with attractive faces as is known to be the case for learning with other types of reward such as juice and money. Subjects showed changes in behavioral ratings to the conditioned stimuli (CS) when comparing post- to preconditioning evaluations, notably for those CSs paired with attractive female faces. We used a simple Rescorla-Wagner learning model to generate a reward-prediction error signal and entered this into a regression analysis with the fMRI data. We found significant prediction error-related activity in the ventral striatum during conditioning with attractive compared with unattractive faces. These findings suggest that an arbitrary stimulus can acquire conditioned value by being paired with pleasant visual stimuli just as with other types of reward such as money or juice. This learning process elicits a reward-prediction error signal in a main target structure of dopamine neurons: the ventral striatum. The findings we describe here may provide insights into the neural mechanisms tapped into by advertisers seeking to influence behavioral preferences by repeatedly exposing consumers to simple associations between products and rewarding visual stimuli such as pretty faces.





2020 ◽  
Vol 46 (Supplement_1) ◽  
pp. S11-S11
Author(s):  
Teresa Katthagen ◽  
Jakob Kaminski ◽  
Andreas Heinz ◽  
Ralph Buchert ◽  
Florian Schlagenhauf

Abstract Background Increased striatal dopamine synthesis capacity (DSC) has consistently been reported in patients with schizophrenia (Sz). However, the functional mechanism translating this into behavior and symptoms remains unclear. It has been proposed that heightened striatal dopamine may blunt dopaminergic reward prediction error (RPE) signaling during reinforcement learning. Methods In this study, we investigated striatal DSC and RPEs and their association in unmedicated Sz and healthy controls. 23 healthy controls (HC) and 20 unmedicated Sz took part in an FDOPA-PET scan measuring DSC and underwent fMRI scanning, where they performed a reversal learning paradigm. We compared groups regarding DSC und neural RPE signals and probed the respective correlation (23 HC and 16 Sz for both measures). Results There was no significant difference between HC and Sz in DSC. Taking into account comorbid alcohol abuse revealed that only patients without such abuse showed elevated DSC in the associative and sensorimotor striatum, while those with abuse did not differ from HC. Patients performed worse during learning, accompanied by a reduced RPE signal in the ventral striatum. In HC, the DSC in the limbic striatum correlated with higher RPE signaling, while there was no significant association in patients. DSC in the associative striatum correlated with higher positive symptoms, and blunted RPE signaling was associated with negative symptoms. Discussion Our results suggest that dopamine modulation of RPE is impaired in schizophrenia. Furthermore, we observed a dissociation with elevated DSC in the associative and sensorimotor striatum contributing to positive symptoms and blunted RPE in the ventral striatum to negative symptoms.



2018 ◽  
Author(s):  
Rachel S. Lee ◽  
Marcelo G. Mattar ◽  
Nathan F. Parker ◽  
Ilana B. Witten ◽  
Nathaniel D. Daw

AbstractAlthough midbrain dopamine (DA) neurons have been thought to primarily encode reward prediction error (RPE), recent studies have also found movement-related DAergic signals. For example, we recently reported that DA neurons in mice projecting to dorsomedial striatum are modulated by choices contralateral to the recording side. Here, we introduce, and ultimately reject, a candidate resolution for the puzzling RPE vs movement dichotomy, by showing how seemingly movement-related activity might be explained by an action-specific RPE. By considering both choice and RPE on a trial-by-trial basis, we find that DA signals are modulated by contralateral choice in a manner that is distinct from RPE, implying that choice encoding is better explained by movement direction. This fundamental separation between RPE and movement encoding may help shed light on the diversity of functions and dysfunctions of the DA system.



2016 ◽  
Vol 18 (1) ◽  
pp. 23-32 ◽  

Reward prediction errors consist of the differences between received and predicted rewards. They are crucial for basic forms of learning about rewards and make us strive for more rewards—an evolutionary beneficial trait. Most dopamine neurons in the midbrain of humans, monkeys, and rodents signal a reward prediction error; they are activated by more reward than predicted (positive prediction error), remain at baseline activity for fully predicted rewards, and show depressed activity with less reward than predicted (negative prediction error). The dopamine signal increases nonlinearly with reward value and codes formal economic utility. Drugs of addiction generate, hijack, and amplify the dopamine reward signal and induce exaggerated, uncontrolled dopamine effects on neuronal plasticity. The striatum, amygdala, and frontal cortex also show reward prediction error coding, but only in subpopulations of neurons. Thus, the important concept of reward prediction errors is implemented in neuronal hardware.



2020 ◽  
Vol 46 (6) ◽  
pp. 1535-1546
Author(s):  
Teresa Katthagen ◽  
Jakob Kaminski ◽  
Andreas Heinz ◽  
Ralph Buchert ◽  
Florian Schlagenhauf

Abstract Increased striatal dopamine synthesis capacity has consistently been reported in patients with schizophrenia. However, the mechanism translating this into behavior and symptoms remains unclear. It has been proposed that heightened striatal dopamine may blunt dopaminergic reward prediction error signaling during reinforcement learning. In this study, we investigated striatal dopamine synthesis capacity, reward prediction errors, and their association in unmedicated schizophrenia patients (n = 19) and healthy controls (n = 23). They took part in FDOPA-PET and underwent functional magnetic resonance imaging (fMRI) scanning, where they performed a reversal-learning paradigm. The groups were compared regarding dopamine synthesis capacity (Kicer), fMRI neural prediction error signals, and the correlation of both. Patients did not differ from controls with respect to striatal Kicer. Taking into account, comorbid alcohol abuse revealed that patients without such abuse showed elevated Kicer in the associative striatum, while those with abuse did not differ from controls. Comparing all patients to controls, patients performed worse during reversal learning and displayed reduced prediction error signaling in the ventral striatum. In controls, Kicer in the limbic striatum correlated with higher reward prediction error signaling, while there was no significant association in patients. Kicer in the associative striatum correlated with higher positive symptoms and blunted reward prediction error signaling was associated with negative symptoms. Our results suggest a dissociation between striatal subregions and symptom domains, with elevated dopamine synthesis capacity in the associative striatum contributing to positive symptoms while blunted prediction error signaling in the ventral striatum related to negative symptoms.



2019 ◽  
Author(s):  
Rachel S Lee ◽  
Marcelo G Mattar ◽  
Nathan F Parker ◽  
Ilana B Witten ◽  
Nathaniel D Daw


2017 ◽  
Vol 114 (52) ◽  
pp. E11303-E11312 ◽  
Author(s):  
Scott A. Schelp ◽  
Katherine J. Pultorak ◽  
Dylan R. Rakowski ◽  
Devan M. Gomez ◽  
Gregory Krzystyniak ◽  
...  

The mesolimbic dopamine system is strongly implicated in motivational processes. Currently accepted theories suggest that transient mesolimbic dopamine release events energize reward seeking and encode reward value. During the pursuit of reward, critical associations are formed between the reward and cues that predict its availability. Conditioned by these experiences, dopamine neurons begin to fire upon the earliest presentation of a cue, and again at the receipt of reward. The resulting dopamine concentration scales proportionally to the value of the reward. In this study, we used a behavioral economics approach to quantify how transient dopamine release events scale with price and causally alter price sensitivity. We presented sucrose to rats across a range of prices and modeled the resulting demand curves to estimate price sensitivity. Using fast-scan cyclic voltammetry, we determined that the concentration of accumbal dopamine time-locked to cue presentation decreased with price. These data confirm and extend the notion that dopamine release events originating in the ventral tegmental area encode subjective value. Using optogenetics to augment dopamine concentration, we found that enhancing dopamine release at cue made demand more sensitive to price and decreased dopamine concentration at reward delivery. From these observations, we infer that value is decreased because of a negative reward prediction error (i.e., the animal receives less than expected). Conversely, enhancing dopamine at reward made demand less sensitive to price. We attribute this finding to a positive reward prediction error, whereby the animal perceives they received a better value than anticipated.



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