Distributional coding of associative learning in discrete populations of midbrain dopamine neurons.

Avvisati R
Kaufmann AK
Young CJ
Portlock GE
Cancemi S
Costa RP
Magill PJ
Dodson PD

Dopamine-producing nerve cells are important for purposeful behaviour. But not all dopamine cells are the same. We recorded the activity of dopamine cells as mice learned to associate a sound with a reward. Different sets of dopamine cells represented sounds, movements, and rewards in varied ways, and sent their signals to different parts of the brain. This diversity helps explain why dopamine cells can play many roles in learning.

Scientific Abstract

Midbrain dopamine neurons are thought to play key roles in learning by conveying the difference between expected and actual outcomes. Recent evidence suggests diversity in dopamine signaling, yet it remains poorly understood how heterogeneous signals might be organized to facilitate the role of downstream circuits mediating distinct aspects of behavior. Here, we investigated the organizational logic of dopaminergic signaling by recording and labeling individual midbrain dopamine neurons during associative behavior. Our findings show that reward information and behavioral parameters are not only heterogeneously encoded but also differentially distributed across populations of dopamine neurons. Retrograde tracing and fiber photometry suggest that populations of dopamine neurons projecting to different striatal regions convey distinct signals. These data, supported by computational modeling, indicate that such distributional coding can maximize dynamic range and tailor dopamine signals to facilitate specialized roles of different striatal regions.

Graphical Abstract from Avvisati et al (2024) Cell Reports
Top left, a traditional view suggesting no diversity of dopamine cell signalling (black lines). Top right, Summary of our data showing diverse signalling by four sets of dopamine cells (in yellow, blue, green and red). Bottom left, the four sets of dopamine cells send axonal projections to different parts of striatum. Bottom right, the four sets of dopamine cells represent information and behaviour in a distributed way.

2024. Cell Rep, 43(4):114080.

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