Prefrontal Regulation of Neuronal Activity in the Ventral Tegmental Area

Jo, Yong Sang; Mizumori, Sheri J. Y.

doi:10.1093/cercor/bhv215

Cited by 37 publications

(43 citation statements)

References 54 publications

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“…While we did not pre-select neurons for recording, it is possible that neurons with different firing correlates were not visible to our electrodes. Nevertheless, the neurons we isolated had waveform and firing correlates similar to putative dopamine neurons in other studies in both rats (Jo et al, 2013; Jo and Mizumori, 2015; Pan et al, 2005) and primates (Bromberg-Martin et al, 2010; Fiorillo et al, 2008; Kobayashi and Schultz, 2008; Morris et al, 2006), recorded in both VTA and substantia nigra pars compacta. Further, most neurons in lateral VTA of the rat are thought to be classical dopamine neurons, meaning that they exhibit the same enzymatic phenotype characteristic of dopamine-releasing neurons in the substantia nigra (Li et al, 2013).…”

Section: Discussionsupporting

confidence: 52%

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Takahashi

Langdon

Niv

et al. 2016

Neuron

115

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Summary Dopamine neurons signal reward prediction errors. This requires accurate reward predictions. It has been suggested that the ventral striatum provides these predictions. Here we tested this hypothesis by recording from putative dopamine neurons in the VTA of rats performing a task in which prediction errors were induced by shifting reward timing or number. In controls, the neurons exhibited error signals in response to both manipulations. However, dopamine neurons in rats with ipsilateral ventral striatal lesions exhibited errors only to changes in number and failed to respond to changes in timing of reward. These results, supported by computational modeling, indicate that predictions about the temporal specificity and the number of expected rewards are dissociable, and that dopaminergic prediction-error signals rely on the ventral striatum for the former but not the latter.

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Section: Discussionsupporting

confidence: 52%

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Takahashi

Langdon

Niv

et al. 2016

Neuron

115

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“…Given evidence that many of these same areas influence dopamine neuron firing generally (Lodge, 2011; Y K Takahashi et al, 2011) and coding of prediction errors specifically (Y S Jo, J Lee, & S J Mizumori, 2013; Jo & Mizumori, 2015; Y K Takahashi et al, 2011), our current findings are perhaps not surprising. However the confirmation that dopamine neurons have access to these inferential predictions, not only in monkeys but also in rats, is important because expands and at the same time makes subtler the potential contributions of these powerful teaching signals to learning.…”

Section: Discussionmentioning

confidence: 55%

Effects of inference on dopaminergic prediction errors depend on orbitofrontal processing.

Takahashi¹,

Stalnaker²,

Roesch³

et al. 2017

Behavioral Neuroscience

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Dopaminergic reward prediction errors in monkeys reflect inferential reward predictions that well-trained animals can make when associative rules change. Here, in a new analysis of previously described data, we test whether dopaminergic error signals in rats are influenced by inferential predictions and whether such effects depend on the orbitofrontal cortex (OFC). Dopamine neurons were recorded from controls or rats with ipsilateral OFC lesions during performance of a choice task in which odor cues signaled the availability of sucrose reward in two wells. To induce prediction errors, we manipulated either the timing or number of rewards delivered in each well across blocks of trials. Importantly, a change in reward at one well predicted a change in reward at the other on later trials. We compared behavior and neural activity on trials when such inference was possible versus trials involving the same reward change when inference was not possible. Rats responded faster when they could infer an increase in reward compared to when the same reward was coming but they could not infer a change. This inferential prediction was reflected in the firing of dopamine neurons in controls, which changed less to unexpected delivery (or omission) of reward and more to the new high-value cue on inference versus non-inference trials. These effects were absent in dopamine neurons recorded in rats with ipsilateral OFC lesions. Thus, dopaminergic error signals recorded in rats are influenced by both experiential and inferential reward predictions, and the effects of inferential predictions depend on OFC.

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“…We found that successful SN/VTA self-regulation is associated with an increased functional 444 coupling between dlPFC regions coding prediction error and the dopaminergic midbrain. This coupling 445 fits well with anatomical connections between dlPFC and the dopaminergic midbrain 19,21 as well as 446 effective connectivity studies on motivation 72 and animal studies on prefrontal regulation of midbrain 447 activity 20,73 . The animal work suggests that prefrontal cortex communicates with dopaminergic 448 neurons primarily indirectly, through inhibitory relay neurons.…”

supporting

confidence: 54%

Individual differences in successful self-regulation of the dopaminergic midbrain

Hellrung

Kirschner

Sulzer

et al. 2019

Preprint

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The dopaminergic midbrain is associated with brain functions, such as reinforcement learning, motivation and decision-making that are often disturbed in neuropsychiatric disease. Previous research has shown that activity in the dopaminergic midbrain can be endogenously modulated via neurofeedback, suggesting potential for non-pharmacological interventions. However, the robustness of endogenous modulation, a requirement for clinical translation, is unclear. Here, we examined how self-modulation capability relates to regulation transfer. Moreover, to elucidate potential mechanisms underlying successful self-regulation, we studied individual prediction error coding, and, during an independent monetary incentive delay (MID) task, individual reward sensitivity. Fifty-nine participants underwent neurofeedback training either in a veridical or inverted feedback group. Successful selfregulation was associated with post-training activity within the cognitive control network and accompanied by decreasing prefrontal prediction error signals and increased prefrontal reward sensitivity in the MID task. The correlative link of dopaminergic self-regulation with individual differences in prefrontal prediction error and reward sensitivity suggests that reinforcement learning contributes to successful self-regulation. Our findings therefore provide new insights in the control of dopaminergic midbrain activity and pave the way to improve neurofeedback training in neuropsychiatric patients. Introduction 1The dopaminergic midbrain, including the ventral tegmental area (VTA) and substantia nigra (SN), plays 2 a crucial role in reward processing, reinforcement learning 1-4 , motivation 5,6 , and decision-making 7 .3 Dysfunctions of the reward system have far-reaching consequences and are associated with the 4 development of several severe psychiatric disease such as addiction 8 and schizophrenia 9,10 . Despite 5 decades of extensive neuroscience and imaging studies which have contributed to an impressive body 6 of knowledge of normal and abnormal reward system function, the neural mechanisms controlling 7 midbrain activity are still not fully understood 11 . One key issue that has received increasing attention 8 is whether humans are able to cognitively control brain activity within the reward system. It has already 9 been shown that both healthy controls 12,13 , and patients with cocaine addiction 14 can learn to regulate 10 SN/VTA activity during real-time functional magnetic resonance imaging (rt-fMRI) neurofeedback 11 training. However, the outcome of primary interest in neurofeedback training is a transfer beyond 12 training itself, i.e., the ability to regulate activity also after training and without feedback. Such transfer 13 is critical for clinical applications, including those involving disorders of the reward system 15 . While 14MacInnes and colleagues 13 observed significant neural transfer effects in the form of increased neural 15 activity and connectivity of the VTA during transfer on the group level, the other two stud...

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Prefrontal Regulation of Neuronal Activity in the Ventral Tegmental Area

Cited by 37 publications

References 54 publications

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Temporal Specificity of Reward Prediction Errors Signaled by Putative Dopamine Neurons in Rat VTA Depends on Ventral Striatum

Effects of inference on dopaminergic prediction errors depend on orbitofrontal processing.

Individual differences in successful self-regulation of the dopaminergic midbrain

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