Sensitivity of Locus Ceruleus Neurons to Reward Value for Goal-Directed Actions

Abstract

The noradrenergic nucleus locus ceruleus (LC) is associated classically with arousal and attention. Recent data suggest that it might also play a role in motivation. To study how LC neuronal responses are related to motivational intensity, we recorded 121 single neurons from two monkeys while reward size (one, two, or four drops) and the manner of obtaining reward (passive vs active) were both manipulated. The monkeys received reward under three conditions: (1) releasing a bar when a visual target changed color; (2) passively holding a bar; or (3) touching and releasing a bar. In the first two conditions, a visual cue indicated the size of the upcoming reward, and, in the third, the reward was constant through each block of 25 trials. Performance levels and lipping intensity (an appetitive behavior) both showed that the monkeys' motivation in the task was related to the predicted reward size. In conditions 1 and 2, LC neurons were activated phasically in relation to cue onset, and this activation strengthened with increasing expected reward size. In conditions 1 and 3, LC neurons were activated before the bar-release action, and the activation weakened with increasing expected reward size but only in task 1. These effects evolved as monkeys progressed through behavioral sessions, because increasing fatigue and satiety presumably progressively decreased the value of the upcoming reward. These data indicate that LC neurons integrate motivationally relevant information: both external cues and internal drives. The LC might provide the impetus to act when the predicted outcome value is low.

Contrasting Roles of Dopamine and Noradrenaline in the Motivational Properties of Social Play Behavior in Rats

“…Noradrenergic neurotransmission has traditionally been implicated in attention and arousal processes (Berridge and Waterhouse, 2003;Aston-Jones and Cohen, 2005), rather than motivation or reward. However, emerging work in rodents (Ventura et al, 2008) and primates (Bouret and Richmond, 2015) has indicated that noradrenergic neurotransmission may also modulate reward processes. Indeed, our recent work implicates prefrontal, amygdala, and habenula noradrenaline in social play behavior (Achterberg et al, 2015), which hints at the possibility that limbic noradrenaline is involved in certain emotional aspects of this behavior.…”

Conservation law for self-paced movements

“…Recent studies indicate that the activity of noradrenergic neurons reflects the effort needed to perform goal-directed actions (33,34): The higher the activity of the noradrenergic neurons in the locus coeruleus, the stronger the action. Amphetamine, which activates both dopamine and adrenergic receptors, greatly enhances movement activity.…”

Mechanisms underlying memory enhancement in humans

“…Strikingly this LC response was shown to be better aligned to the movement compared to the stimuli presentation in and was not elicited either in the present of a response inhibition cue, or with the successful withholding of the movement (Kalwani et al, 2014). Interestingly, this LC response is elicited regardless of speed of response (Bouret & Richmond, 2009;Bouret & Richmond, 2015;, correctness Kalwani et al, 2014) or reward expectation -LC fires with action even when the animal did not anticipate reward- (Bouret & Richmond, 2015;Clayton et al, 2004). Furthermore the anticipation of effort needed to perform an action has been also shown to modulate LC firing suggesting that LC is also signalling the energy requirements of the movement (Varazzani et al, 2015).…”

“…Interestingly, although a significant proportion of individual neurons displayed a firing modulation related to reward before the feedback in self-initiated trials, there was no modulation related to the reward size at the population level. Thus, the effects observed on individual neurons are not coherent enough to emerge at the level of the population (Bouret & Richmond, 2015).…”

“…Recent single-unit recordings of the LC in non-human primates demonstrate increased activity before the onset of the movement or with the onset of the stimuli presentation led to the suggestion that LC phasic response is driven by the outcome of a decision process and the commitment to act (Bouret, & Richmond, 2009;Bouret & Richmond, 2015;Clayton et al, 2004;Kalwani et al, 2014;Pavlenko & Kulichenko, 2003;Varazzani et al, 2015). It could be possible that later components of the LC activation would produce NE liberation after motor circuits are already activated.…”