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Dissociable dopamine dynamics for learning and motivation.

ABSTRACT: The dopamine projection from ventral tegmental area (VTA) to nucleus accumbens (NAc) is critical for motivation to work for rewards and reward-driven learning. How dopamine supports both functions is unclear. Dopamine cell spiking can encode prediction errors, which are vital learning signals in computational theories of adaptive behaviour. By contrast, dopamine release ramps up as animals approach rewards, mirroring reward expectation. This mismatch might reflect differences in behavioural tasks, slower changes in dopamine cell spiking or spike-independent modulation of dopamine release. Here we compare spiking of identified VTA dopamine cells with NAc dopamine release in the same decision-making task. Cues that indicate an upcoming reward increased both spiking and release. However, NAc core dopamine release also covaried with dynamically evolving reward expectations, without corresponding changes in VTA dopamine cell spiking. Our results suggest a fundamental difference in how dopamine release is regulated to achieve distinct functions: broadcast burst signals promote learning, whereas local control drives motivation.

SUBMITTER: Mohebi A

PROVIDER: S-EPMC6555489 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Dissociable dopamine dynamics for learning and motivation.

Mohebi Ali A Pettibone Jeffrey R JR Hamid Arif A AA Wong Jenny-Marie T JT Vinson Leah T LT Patriarchi Tommaso T Tian Lin L Kennedy Robert T RT Berke Joshua D JD

Nature 20190522 7759

The dopamine projection from ventral tegmental area (VTA) to nucleus accumbens (NAc) is critical for motivation to work for rewards and reward-driven learning. How dopamine supports both functions is unclear. Dopamine cell spiking can encode prediction errors, which are vital learning signals in computational theories of adaptive behaviour. By contrast, dopamine release ramps up as animals approach rewards, mirroring reward expectation. This mismatch might reflect differences in behavioural task ...[more]

PMID: 31118513

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Project description:BackgroundIn a changing environment, a challenge for the brain is to flexibly guide adaptive behavior towards survival. Complex behavior and the underlying neural computations emerge from the structural components of the brain across many levels: circuits, cells, and ultimately the signaling complex of proteins at synapses. In line with this logic, dynamic modification of synaptic strength or synaptic plasticity is widely considered the cellular level implementation for adaptive behavior such as learning and memory. Predominantly expressed at excitatory synapses, the postsynaptic cell-adhesion molecule neuroligin-1 (Nlgn1) forms trans-synaptic complexes with presynaptic neurexins. Extensive evidence supports that Nlgn1 is essential for NMDA receptor transmission and long-term potentiation (LTP), both of which are putative synaptic mechanisms underlying learning and memory. Here, employing a comprehensive battery of touchscreen-based cognitive assays, we asked whether impaired NMDA receptor transmission and LTP in mice lacking Nlgn1 does in fact disrupt decision-making. To this end, we addressed two key decision problems: (i) the ability to learn and exploit the associative structure of the environment and (ii) balancing the trade-off between potential rewards and costs, or positive and negative utilities of available actions.ResultsWe found that the capacity to acquire complex associative structures and adjust learned associations was intact. However, loss of Nlgn1 alters motivation leading to a reduced willingness to overcome effort cost for reward and an increased willingness to exert effort to escape an aversive situation. We suggest Nlgn1 may be important for balancing the weighting on positive and negative utilities in reward-cost trade-off.ConclusionsOur findings update canonical views of this key synaptic molecule in behavior and suggest Nlgn1 may be essential for regulating distinct cognitive processes underlying action selection. Our data demonstrate that learning and motivational computations can be dissociated within the same animal model, from a detailed behavioral dissection. Further, these results highlight the complexities in mapping synaptic mechanisms to their behavioral consequences, and the future challenge to elucidate how complex behavior emerges through different levels of neural hardware.

Dataset Information

Dissociable dopamine dynamics for learning and motivation.

Publications

Dissociable dopamine dynamics for learning and motivation.

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