Microstimulation of the Human Substantia Nigra Alters Reinforcement Learning

Ramayya, Ashwin G.; Misra, Amrit; Baltuch, Gordon H.; Kahana, Michael J.

doi:10.1523/jneurosci.5445-13.2014

Cited by 27 publications

(47 citation statements)

References 41 publications

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“…There is, however, a growing body of literature implicating the substantia nigra dopamine neurons in the rewarding aspects of cocaine (Ilango et al, 2014;Ramayya et al, 2014;Rossi et al, 2013;Wise, 2009). This study suggests that plasticity of dopamine neurons in the substantia nigra can contribute at a cellular level to cocaine-induced modulation.…”

Section: Discussionmentioning

confidence: 99%

Cocaine Decreases Metabotropic Glutamate Receptor mGluR1 Currents in Dopamine Neurons by Activating mGluR5

Kramer

Williams

2015

Neuropsychopharmacol

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Midbrain dopamine neurons are important mediators of reward and movement and are sensitive to cocaine-induced plasticity. After even a single injection of cocaine, there is an increase in AMPA-dependent synaptic transmission. The present study examines cocaine-induced plasticity of mGluR-dependent currents in dopamine neurons in the substantia nigra. Activation of mGluR1 and mGluR5 resulted in a mixture of inward and outward currents mediated by a nonselective cation conductance and a calcium-activated potassium conductance (SK), respectively. A single injection of cocaine decreased the current activated by mGluR1 in dopamine neurons, and it had no effect on the size of the mGluR5-mediated current. When the injection of cocaine was preceded by treatment of the animals with a blocker of mGluR5 receptors (MPEP), cocaine no longer decreased the mGluR1 current. Thus, the activation of mGluR5 was required for the cocaine-mediated suppression of mGluR1-mediated currents in dopamine neurons. The results support the hypothesis that mGluR5 coordinates a reduction in mGluR1 functional activity after cocaine treatment.

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Section: Discussionmentioning

confidence: 99%

Cocaine Decreases Metabotropic Glutamate Receptor mGluR1 Currents in Dopamine Neurons by Activating mGluR5

Kramer

Williams

2015

Neuropsychopharmacol

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“…Whether phasic activity in SNc DA neurons also contributes to reward prediction learning remains uncertain. Based on their different striatal targets, distinct contributions to learning have been proposed for VTA and SNc DA neurons [8–10]; specifically, that VTA-DA signals contribute to reward predictions while SNc-DA signals contribute to action reinforcement [11, 12]. …”

Section: Introductionmentioning

confidence: 99%

Ventral Tegmental Dopamine Neurons Participate in Reward Identity Predictions

et al. 2019

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SUMMARY Dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SNc) encode reward prediction errors (RPEs) and are proposed to mediate error-driven learning. However the learning strategy engaged by DA-RPEs remains controversial. RPEs might imbue cue/actions with pure value, independently of representations of their associated outcome. Alternatively, RPEs might promote learning about the sensory features (the identity) of the rewarding outcome. Here we show that although both VTA and SNc DA neuron activation reinforces instrumental responding, only VTA DA neuron activation during consumption of expected sucrose reward restores error-driven learning and promotes formation of a new cue➔sucrose association. Critically, expression of VTA DA-dependent Pavlovian associations is abolished following sucrose devaluation, a signature of identity-based learning. These findings reveal that activation of VTA- or SNc-DA neurons engages largely dissociable learning processes with VTA-DA neurons capable of participating outcome-specific predictive learning, while the role of SNc-DA neurons appears limited to reinforcement of instrumental responses.

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“…For example, functional neuroimaging studies have identified a specialized group of brain regions that encode reward prediction errors (Berns et al, 2001; McClure et al, 2003; Pessiglione et al, 2006; Montague et al, 2006; Rutledge et al, 2010; Bartra et al, 2013). Several of these regions (e.g., ventral striatum, medial prefrontal cortex) receive prominent inputs from midbrain dopaminergic (DA) neurons, a neural population known to be functionally important for reinforcement learning in animals (Schultz et al, 1997; Reynolds et al, 2001) and humans (Zaghloul et al, 2009; Ramayya et al, 2014a). …”

Section: Introductionmentioning

confidence: 99%

Expectation modulates neural representations of valence throughout the human brain

2015

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The brain's sensitivity to unexpected gains or losses plays an important role in our ability to learn new behaviors (Rescorla and Wagner, 1972; Sutton and Barto, 1990). Recent work suggests that gains and losses are ubiquitously encoded throughout the human brain (Vickery et al., 2011), however, the extent to which reward expectation modulates these valence representations is not known. To address this question we analyzed recordings from 4,306 intracranially implanted electrodes in 39 neurosurgical patients as they performed a two-alternative probability learning task. Using high-frequency activity (HFA, 70-200 Hz) as an indicator of local firing rates, we found that expectation modulated reward-related neural activity in widespread brain regions, including regions that receive sparse inputs from midbrain dopaminergic neurons. The strength of unexpected gain signals predicted subjects’ abilities to encode stimulus-reward associations. Thus, neural signals that are functionally related to learning are widely distributed throughout the human brain.

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Microstimulation of the Human Substantia Nigra Alters Reinforcement Learning

Cited by 27 publications

References 41 publications

Cocaine Decreases Metabotropic Glutamate Receptor mGluR1 Currents in Dopamine Neurons by Activating mGluR5

Cocaine Decreases Metabotropic Glutamate Receptor mGluR1 Currents in Dopamine Neurons by Activating mGluR5

Ventral Tegmental Dopamine Neurons Participate in Reward Identity Predictions

Expectation modulates neural representations of valence throughout the human brain

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