scholarly journals Dopamine neuron ensembles signal the content of sensory prediction errors

2019 ◽  
Author(s):  
Thomas A. Stalnaker ◽  
James D. Howard ◽  
Yuji K. Takahashi ◽  
Samuel J. Gershman ◽  
Thorsten Kahnt ◽  
...  
Keyword(s):  
Neural Activity ◽  
Prediction Error ◽  
Sensory Information ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Bold Response ◽  
Dopamine System ◽  
Sensory Event ◽  
Specific Teaching ◽  
Sensory Prediction

AbstractDopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in individual neuron or average neural activity. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning.

scholarly journals Dopamine neuron ensembles signal the content of sensory prediction errors

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Thomas A Stalnaker ◽  
James D Howard ◽  
Yuji K Takahashi ◽  
Samuel J Gershman ◽  
Thorsten Kahnt ◽  
...  
Keyword(s):  
Associative Learning ◽  
Prediction Error ◽  
Sensory Information ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Bold Response ◽  
Dopamine System ◽  
Sensory Event ◽  
Specific Teaching ◽  
Sensory Prediction

Dopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in the activity of individual neurons or population averages. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning.

scholarly journals Rethinking dopamine as generalized prediction error

2017 ◽  
Author(s):  
Matthew P.H. Gardner ◽  
Geoffrey Schoenbaum ◽  
Samuel J. Gershman
Keyword(s):  
Reinforcement Learning ◽  
Prediction Error ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Model Free ◽  
Reward Prediction ◽  
Midbrain Dopamine ◽  
Sensory Prediction ◽  
Lines Of Evidence ◽  
Midbrain Dopamine Neurons

AbstractMidbrain dopamine neurons are commonly thought to report a reward prediction error, as hypothesized by reinforcement learning theory. While this theory has been highly successful, several lines of evidence suggest that dopamine activity also encodes sensory prediction errors unrelated to reward. Here we develop a new theory of dopamine function that embraces a broader conceptualization of prediction errors. By signaling errors in both sensory and reward predictions, dopamine supports a form of reinforcement learning that lies between model-based and model-free algorithms. This account remains consistent with current canon regarding the correspondence between dopamine transients and reward prediction errors, while also accounting for new data suggesting a role for these signals in phenomena such as sensory preconditioning and identity unblocking, which ostensibly draw upon knowledge beyond reward predictions.

scholarly journals Rethinking dopamine as generalized prediction error

2018 ◽  
Vol 285 (1891) ◽  
pp. 20181645 ◽  
Author(s):  
Matthew P. H. Gardner ◽  
Geoffrey Schoenbaum ◽  
Samuel J. Gershman
Keyword(s):  
Reinforcement Learning ◽  
Prediction Error ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Model Free ◽  
Reward Prediction ◽  
Midbrain Dopamine ◽  
Sensory Prediction ◽  
Lines Of Evidence ◽  
Midbrain Dopamine Neurons

Midbrain dopamine neurons are commonly thought to report a reward prediction error (RPE), as hypothesized by reinforcement learning (RL) theory. While this theory has been highly successful, several lines of evidence suggest that dopamine activity also encodes sensory prediction errors unrelated to reward. Here, we develop a new theory of dopamine function that embraces a broader conceptualization of prediction errors. By signalling errors in both sensory and reward predictions, dopamine supports a form of RL that lies between model-based and model-free algorithms. This account remains consistent with current canon regarding the correspondence between dopamine transients and RPEs, while also accounting for new data suggesting a role for these signals in phenomena such as sensory preconditioning and identity unblocking, which ostensibly draw upon knowledge beyond reward predictions.

scholarly journals Reward prediction error in the ERP following unconditioned aversive stimuli

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Harry J. Stewardson ◽  
Thomas D. Sambrook
Keyword(s):  
Reinforcement Learning ◽  
Prediction Error ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Temporal Difference ◽  
Dopamine System ◽  
Reward Prediction Error ◽  
Reward Prediction ◽  
Midbrain Dopamine ◽  
Human Participants

AbstractReinforcement learning in humans and other animals is driven by reward prediction errors: deviations between the amount of reward or punishment initially expected and that which is obtained. Temporal difference methods of reinforcement learning generate this reward prediction error at the earliest time at which a revision in reward or punishment likelihood is signalled, for example by a conditioned stimulus. Midbrain dopamine neurons, believed to compute reward prediction errors, generate this signal in response to both conditioned and unconditioned stimuli, as predicted by temporal difference learning. Electroencephalographic recordings of human participants have suggested that a component named the feedback-related negativity (FRN) is generated when this signal is carried to the cortex. If this is so, the FRN should be expected to respond equivalently to conditioned and unconditioned stimuli. However, very few studies have attempted to measure the FRN’s response to unconditioned stimuli. The present study attempted to elicit the FRN in response to a primary aversive stimulus (electric shock) using a design that varied reward prediction error while holding physical intensity constant. The FRN was strongly elicited, but earlier and more transiently than typically seen, suggesting that it may incorporate other processes than the midbrain dopamine system.

scholarly journals Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Brain ◽  
2019 ◽  
Vol 142 (3) ◽  
pp. 662-673 ◽  
Author(s):  
Aaron L Wong ◽  
Cherie L Marvel ◽  
Jordan A Taylor ◽  
John W Krakauer
Keyword(s):  
Prediction Error ◽  
Poor Performance ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Cerebellar Disease ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

Abstract Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed—by allowing vision of the hand, which eliminates sensory-prediction errors—patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction error signal to zero. We demonstrated in younger healthy control subjects that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with cerebellar degeneration could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed (although they could not improve beyond what they retrieved), and retain it for at least 1 year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age 18–33 years), likely due to age-related reductions in spatial and working memory. Patients also failed to generalize, i.e. they were unable to adopt analogous aiming strategies in response to novel rotations. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction error-based learning—even when this system is impaired in patients with cerebellar disease. The persistence of sensory-prediction error-based learning effectively suppresses a switch to target error-based learning, which perhaps explains the unexpectedly poor performance by patients with cerebellar degeneration in visuomotor adaptation tasks.

Overlapping Prediction Errors in Dorsal Striatum During Instrumental Learning With Juice and Money Reward in the Human Brain

2009 ◽  
Vol 102 (6) ◽  
pp. 3384-3391 ◽  
Author(s):  
Vivian V. Valentin ◽  
John P. O'Doherty
Keyword(s):  
Prediction Error ◽  
Apple Juice ◽  
Instrumental Learning ◽  
Dorsal Striatum ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Imaging Data ◽  
Different Types ◽  
Monetary Gain ◽  
Reinforcement Learning Model

Prediction error signals have been reported in human imaging studies in target areas of dopamine neurons such as ventral and dorsal striatum during learning with many different types of reinforcers. However, a key question that has yet to be addressed is whether prediction error signals recruit distinct or overlapping regions of striatum and elsewhere during learning with different types of reward. To address this, we scanned 17 healthy subjects with functional magnetic resonance imaging while they chose actions to obtain either a pleasant juice reward (1 ml apple juice), or a monetary gain (5 cents) and applied a computational reinforcement learning model to subjects' behavioral and imaging data. Evidence for an overlapping prediction error signal during learning with juice and money rewards was found in a region of dorsal striatum (caudate nucleus), while prediction error signals in a subregion of ventral striatum were significantly stronger during learning with money but not juice reward. These results provide evidence for partially overlapping reward prediction signals for different types of appetitive reinforcers within the striatum, a finding with important implications for understanding the nature of associative encoding in the striatum as a function of reinforcer type.

scholarly journals Stimulus Representation and the Timing of Reward-Prediction Errors in Models of the Dopamine System

2008 ◽  
Vol 20 (12) ◽  
pp. 3034-3054 ◽  
Author(s):  
Elliot A. Ludvig ◽  
Richard S. Sutton ◽  
E. James Kehoe
Keyword(s):  
Learning Algorithm ◽  
Full Range ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Dopamine System ◽  
Stimulus Representation ◽  
Reward Prediction ◽  
Future Reward ◽  
Temporal Generalization ◽  
External Stimuli

The phasic firing of dopamine neurons has been theorized to encode a reward-prediction error as formalized by the temporal-difference (TD) algorithm in reinforcement learning. Most TD models of dopamine have assumed a stimulus representation, known as the complete serial compound, in which each moment in a trial is distinctly represented. We introduce a more realistic temporal stimulus representation for the TD model. In our model, all external stimuli, including rewards, spawn a series of internal microstimuli, which grow weaker and more diffuse over time. These microstimuli are used by the TD learning algorithm to generate predictions of future reward. This new stimulus representation injects temporal generalization into the TD model and enhances correspondence between model and data in several experiments, including those when rewards are omitted or received early. This improved fit mostly derives from the absence of large negative errors in the new model, suggesting that dopamine alone can encode the full range of TD errors in these situations.

scholarly journals Positive reward prediction errors strengthen incidental memory encoding

2018 ◽  
Author(s):  
Anthony I. Jang ◽  
Matthew R. Nassar ◽  
Daniel G. Dillon ◽  
Michael J. Frank
Keyword(s):  
Prediction Error ◽  
Memory Systems ◽  
Prediction Errors ◽  
Memory Encoding ◽  
Dopamine System ◽  
Reward Prediction Error ◽  
Reward Prediction ◽  
Incidental Memory ◽  
Episodic Memories ◽  
The Impact

AbstractThe dopamine system is thought to provide a reward prediction error signal that facilitates reinforcement learning and reward-based choice in corticostriatal circuits. While it is believed that similar prediction error signals are also provided to temporal lobe memory systems, the impact of such signals on episodic memory encoding has not been fully characterized. Here we develop an incidental memory paradigm that allows us to 1) estimate the influence of reward prediction errors on the formation of episodic memories, 2) dissociate this influence from other factors such as surprise and uncertainty, 3) test the degree to which this influence depends on temporal correspondence between prediction error and memoranda presentation, and 4) determine the extent to which this influence is consolidation-dependent. We find that when choosing to gamble for potential rewards during a primary decision making task, people encode incidental memoranda more strongly even though they are not aware that their memory will be subsequently probed. Moreover, this strengthened encoding scales with the reward prediction error, and not overall reward, experienced selectively at the time of memoranda presentation (and not before or after). Finally, this strengthened encoding is identifiable within a few minutes and is not substantially enhanced after twenty-four hours, indicating that it is not consolidation-dependent. These results suggest a computationally and temporally specific role for putative dopaminergic reward prediction error signaling in memory formation.

scholarly journals Dopamine transients delivered in learning contexts do not act as model-free prediction errors

2019 ◽  
Author(s):  
Melissa J. Sharpe ◽  
Hannah M. Batchelor ◽  
Lauren E. Mueller ◽  
Chun Yun Chang ◽  
Etienne J.P. Maes ◽  
...  
Keyword(s):  
Reinforcement Learning ◽  
Associative Learning ◽  
Prediction Error ◽  
Error Term ◽  
Neural Correlates ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Model Free ◽  
Reward Prediction ◽  
Excess Value

AbstractDopamine neurons fire transiently in response to unexpected rewards. These neural correlates are proposed to signal the reward prediction error described in model-free reinforcement learning algorithms. This error term represents the unpredicted or ‘excess’ value of the rewarding event. In model-free reinforcement learning, this value is then stored as part of the learned value of any antecedent cues, contexts or events, making them intrinsically valuable, independent of the specific rewarding event that caused the prediction error. In support of equivalence between dopamine transients and this model-free error term, proponents cite causal optogenetic studies showing that artificially induced dopamine transients cause lasting changes in behavior. Yet none of these studies directly demonstrate the presence of cached value under conditions appropriate for associative learning. To address this gap in our knowledge, we conducted three studies where we optogenetically activated dopamine neurons while rats were learning associative relationships, both with and without reward. In each experiment, the antecedent cues failed to acquired value and instead entered into value-independent associative relationships with the other cues or rewards. These results show that dopamine transients, constrained within appropriate learning situations, support valueless associative learning.

scholarly journals Dopamine reward prediction error coding

2016 ◽  
Vol 18 (1) ◽  
pp. 23-32 ◽  
Keyword(s):  
Prediction Error ◽  
Dopamine Neurons ◽  
Prediction Errors ◽  
Reward Prediction Error ◽  
Reward Prediction ◽  
Negative Prediction ◽  
Baseline Activity ◽  
Error Coding ◽  
Reward Value ◽  
Dopamine Signal

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.

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