Topographic distinction in long-term value signals between presumed dopamine neurons and presumed striatal projection neurons in behaving monkeys

Kazuki Enomoto,Hitoshi Inokawa,Hiroshi Yamada,Naoyuki Matsumoto,Minoru Kimura

doi:10.1038/s41598-020-65914-0

Abstract

Nigrostriatal dopamine (DA) projections are anatomically organized along the dorsolateral-ventromedial axis, conveying long-term value signals to the striatum for shaping actions toward multiple future rewards. The present study examines whether the topographic organization of long-term value signals are observed upon activity of presumed DA neurons and presumed striatal projection neurons (phasically active neurons, PANs), as predicted based on anatomical literature. Our results indicate that DA neurons in the dorsolateral midbrain encode long-term value signals on a short timescale, while ventromedial midbrain DA neurons encode such signals on a relatively longer timescale. Activity of the PANs in the dorsal striatum is more heterogeneous for encoding long-term values, although significant differences in long-term value signals were observed between the caudate nucleus and putamen. These findings suggest that topographic DA signals for long-term values are not simply transferred to striatal neurons, possibly due to the contribution of other projections to the striatum.

Highlights

Nigrostriatal dopamine (DA) projections are anatomically organized along the dorsolateralventromedial axis, conveying long-term value signals to the striatum for shaping actions toward multiple future rewards
We examine the heterogeneity of long-term value signals in terms of topography by analyzing the recording locations of neurons in our datasets, in which we have already demonstrated that DA neurons and phasically active neurons (PANs) encode long-term values using the same behavioral task[5,31]
Two prior studies conducted in our laboratory have shown that DA neurons and PANs encode the expected values of multiple future rewards during a series of choices[5,31]

Summary

Introduction

Nigrostriatal dopamine (DA) projections are anatomically organized along the dorsolateralventromedial axis, conveying long-term value signals to the striatum for shaping actions toward multiple future rewards. Previous findings suggest that the values of immediate rewards, and long-term values of multiple future rewards (i.e. those associated with multiple future rewards through a series of actions) are learned based on signals from midbrain dopamine (DA) neurons, which convey reward values to cortical and sub-cortical structures[1,2,3,4,5] It remains unclear how DA value signals are reflected in neuronal activity within these target brain regions. We examined (1) whether the long-term value signals of DA neurons exhibit a topography along the dorsolateral-ventromedial axis; (2) whether PANs exhibit topographic differences in the encoding of long-term values; (3) whether the topographical organization patterns of DA neurons and PANs reflect that predicted by anatomical literature[15,16]. Their topographic characteristics did not completely align with the nigrostriatal anatomical projections, suggesting that additional contributions from other networks are likely involved

Methods

Results

Conclusion