Research Article

Local D2- to D1-neuron transmodulation updates goal-directed learning in the striatum

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Science  31 Jan 2020:
Vol. 367, Issue 6477, pp. 549-555
DOI: 10.1126/science.aaz5751

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A learning mechanism in the striatum

An intriguing characteristic of the striatum is the random spatial distribution and high degree of intermingling between expression of dopamine receptor types 1 (D1) and 2 (D2) within striatal projection neurons (SPNs). The resulting highly entropic mosaic extends through a homogeneous space and is mostly devoid of histological boundaries. The rules established locally by D1- and D2-expressing SPNs (D1-SPNs and D2-SPNs) are thus likely critical in defining how functional territories develop throughout the striatum. Matamales et al. found that activated D2-SPNs access and modify developing behavioral programs encoded by regionally defined ensembles of transcriptionally active D1-SPNs. This process is slow because it depends on the molecular integration of additive neuro-modulatory signals. However, with time, it creates the regional functional boundaries that are necessary to identify and shape specific learning in the striatum.

Science, this issue p. 549

Abstract

Extinction learning allows animals to withhold voluntary actions that are no longer related to reward and so provides a major source of behavioral control. Although such learning is thought to depend on dopamine signals in the striatum, the way the circuits that mediate goal-directed control are reorganized during new learning remains unknown. Here, by mapping a dopamine-dependent transcriptional activation marker in large ensembles of spiny projection neurons (SPNs) expressing dopamine receptor type 1 (D1-SPNs) or 2 (D2-SPNs) in mice, we demonstrate an extensive and dynamic D2- to D1-SPN transmodulation across the striatum that is necessary for updating previous goal-directed learning. Our findings suggest that D2-SPNs suppress the influence of outdated D1-SPN plasticity within functionally relevant striatal territories to reshape volitional action.

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