Noradrenergic But Not Dopaminergic Neurons Signal Task State Changes and Predict Reengagement After a Failure

Abstract

The two catecholamines, noradrenaline and dopamine, have been shown to play comparable roles in behavior. Both noradrenergic and dopaminergic neurons respond to cues predicting reward availability and novelty. However, even though both are thought to be involved in motivating actions, their roles in motivation have seldom been directly compared. We therefore examined the activity of putative noradrenergic neurons in the locus coeruleus and putative midbrain dopaminergic neurons in monkeys cued to perform effortful actions for rewards. The activity in both regions correlated with engagement with a presented option. By contrast, only noradrenaline neurons were also (i) predictive of engagement in a subsequent trial following a failure to engage and (ii) more strongly activated in nonrepeated trials, when cues indicated a new task condition. This suggests that while both catecholaminergic neurons are involved in promoting action, noradrenergic neurons are sensitive to task state changes, and their influence on behavior extends beyond the immediately rewarded action.

Locus Coeruleus Norepinephrine in Learned Behavior: Anatomical Modularity and Spatiotemporal Integration in Targets

“…Recordings or pharmacological manipulations of phasic NE activity suggest a dual involvement in behavior and cognition. First, LC activation is critical for sustained attention, as its phasic activity correlates with behavioral responses in learned behaviors ( Bouret and Sara, 2004 ; Clayton et al, 2004 ; Rajkowski et al, 2004 ; Bouret and Richmond, 2009 , 2015 ; Kalwani et al, 2014 ; Varazzani et al, 2015 ; Jahn et al, 2020 ). Non-targeted recordings in the LC show a transient increase in firing rate coinciding with behavioral response in tasks involving operant or instrumental conditioning.…”

Locus coeruleus neurons encode the subjective difficulty of triggering and executing actions

“…For cognitive effort, we took advantage of the fact that monkeys tend to disengage from single-option tasks when the outcome value is low, even if erroneous trials are repeated [3][4][5][39][40][41][42]. Note that a slightly different intuition would be that monkeys simply engage in the task as a function of expected outcome value, such that in low value conditions, they fail to engage and/or wait for a better option.…”

“…The locus coeruleus noradrenergic (LC/NA) system is involved in various functions such as arousal, stress, attention, and decision-making (see [1] for review). We recently proposed a role in effort processing [2][3][4][5]. Effort encompasses multiple notions, but it could be generally defined as a mobilization of resources to face challenges [6,7].…”

The ascending arousal system shapes low-dimensional neural dynamics to mediate awareness of intrinsic cognitive states

“…3A). At this point, there is a mismatch between expectation and conscious awareness, which is an internal state that has been previously linked to the activation of the noradrenergic system, both in theoretical 36,37 and computational 38 work. Based on these studies, we predicted that the switch in internal conscious awareness would be facilitated by increases in locus coeruleus-mediated integration and subsequent reconfiguration of low-dimensional brain states.…”