Motivational Salience Signal in the Basal Forebrain Is Coupled with Faster and More Precise Decision Speed

The survival of animals depends critically on prioritizing responses to motivationally salient stimuli. While it is generally believed that motivational salience increases decision speed, the quantitative relationship between motivational salience and decision speed, measured by reaction time (RT), remains unclear. Here we show that the neural correlate of motivational salience in the basal forebrain (BF), defined independently of RT, is coupled with faster and also more precise decision speed. In rats performing a reward-biased simple RT task, motivational salience was encoded by BF bursting response that occurred before RT. We found that faster RTs were tightly coupled with stronger BF motivational salience signals. Furthermore, the fraction of RT variability reflecting the contribution of intrinsic noise in the decision-making process was actively suppressed in faster RT distributions with stronger BF motivational salience signals. Artificially augmenting the BF motivational salience signal via electrical stimulation led to faster and more precise RTs and supports a causal relationship. Together, these results not only describe for the first time, to our knowledge, the quantitative relationship between motivational salience and faster decision speed, they also reveal the quantitative coupling relationship between motivational salience and more precise RT. Our results further establish the existence of an early and previously unrecognized step in the decision-making process that determines both the RT speed and variability of the entire decision-making process and suggest that this novel decision step is dictated largely by the BF motivational salience signal. Finally, our study raises the hypothesis that the dysregulation of decision speed in conditions such as depression, schizophrenia, and cognitive aging may result from the functional impairment of the motivational salience signal encoded by the poorly understood noncholinergic BF neurons. Author Summary Humans and animals face the constant challenge of identifying the subset of incoming sensory stimuli that are most behaviorally relevant and prioritizing behavioral responses accordingly. Critical to this decision is the ability to determine whether a stimulus is motivationally salientthat is, whether the stimulus predicts important behavioral outcomes such as reward or punishment. While it is generally assumed that motivational salience is related to faster decision speed and shorter reaction time, it remains unclear how motivational salience actually modulates the decision-making process. This study investigates how the motivational salience signal in the basal forebrain controls the fundamental properties of the decision-making processdecision speed and its variability. In rats performing a reward-biased simple reaction time task, we show that the basal forebrain motivational salience signal is associated with a faster and also precise decision speed. In support of a causal role for this association, artificially augmenting this basal forebrain motivational salience signal by electrical stimulation also leads to faster and more precise reaction times. These results suggest that decision speed and its variability are jointly determined by an early and previously unrecognized step in the decision-making process, dictated largely by the motivational salience signal encoded by poorly understood noncholinergic neurons in the basal forebrain.