Novelty, Salience, and Surprise Timing Are Signaled by Neurons in the Basal Forebrain

Summary The basal forebrain (BF) is a principal source of modulation of the neocortex [ 1 , 2 , 3 , 4 , 5 , 6 ] and is thought to regulate cognitive functions such as attention, motivation, and learning by broadcasting information about salience [ 2 , 3 , 5 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 ]. However, events can be salient for multiple reasons—such as novelty, surprise, or reward prediction errors [ 20 , 21 , 22 , 23 , 24 ]—and to date, precisely which salience-related information the BF broadcasts is unclear. Here, we report that the primate BF contains at least two types of neurons that often process salient events in distinct manners: one with phasic burst responses to cues predicting salient events and one with ramping activity anticipating such events. Bursting neurons respond to cues that convey predictions about the magnitude, probability, and timing of primary reinforcements. They also burst to the reinforcement itself, particularly when it is unexpected. However, they do not have a selective response to reinforcement omission (the unexpected absence of an event). Thus, bursting neurons do not convey value-prediction errors but do signal surprise associated with external events. Indeed, they are not limited to processing primary reinforcement: they discriminate fully expected novel visual objects from familiar objects and respond to object-sequence violations. In contrast, ramping neurons predict the timing of many salient, novel, and surprising events. Their ramping activity is highly sensitive to the subjects’ confidence in event timing and on average encodes the subjects’ surprise after unexpected events occur. These data suggest that the primate BF contains mechanisms to anticipate the timing of a diverse set of important external events (via ramping activity) and to rapidly deploy cognitive resources when these events occur (via short latency bursting).