Tonic firing mode of midbrain dopamine neurons continuously tracks reward values changing moment-by-moment.

Yawei Wang,Jun Kunimatsu,Hiroshi Yamada,Masayuki Matsumoto,Osamu Toyoshima

doi:10.7554/elife.63166

Abstract

Animal behavior is regulated based on the values of future rewards. The phasic activity of midbrain dopamine neurons signals these values. Because reward values often change over time, even on a subsecond-by-subsecond basis, appropriate behavioral regulation requires continuous value monitoring. However, the phasic dopamine activity, which is sporadic and has a short duration, likely fails continuous monitoring. Here, we demonstrate a tonic firing mode of dopamine neurons that effectively tracks changing reward values. We recorded dopamine neuron activity in monkeys during a Pavlovian procedure in which the value of a cued reward gradually increased or decreased. Dopamine neurons tonically increased and decreased their activity as the reward value changed. This tonic activity was evoked more strongly by non-burst spikes than burst spikes producing a conventional phasic activity. Our findings suggest that dopamine neurons change their firing mode to effectively signal reward values in a given situation.

Highlights

We often experience situations in which the value of future rewards changes on a moment-bymoment basis
Pavlovian procedure in which the value of a cued reward gradually changed We designed a Pavlovian procedure with three different conditions (Figure 1A–C) and applied it to two macaque monkeys
In the first condition, the green area was minimal at the beginning and gradually increased (3.8 ̊/s), that is, the reward value gradually increased (0.082 ml/s) (Video 1)

Summary

Introduction

We often experience situations in which the value of future rewards changes on a moment-bymoment basis. Midbrain dopamine neurons have been considered to function as a key neural substrate that signals reward values and regulates reward-seeking behavior. These neurons respond to rewards and reward-predicting cues with phasic activity (Bayer and Glimcher, 2005; Cohen et al, 2012; Kawagoe et al, 2004; Morris et al, 2004; Satoh et al, 2003; Schultz, 1998). The cue-evoked phasic activity of dopamine neurons has been reported to reflect the value of cued rewards (Matsumoto and Hikosaka, 2009; Roesch et al, 2007; Tobler et al, 2005) and has recently been demonstrated to influence behavior associated with cued rewards (Maes et al, 2020; Morrens et al, 2020)

Methods

Results

Discussion

Conclusion