Amygdala Neural Encoding of the Absence of Reward during Extinction

The basolateral amygdala complex (BLA) has been identified as a critical structure mediating fear extinction. However, little is known about the functional role of neurons in the BLA during the extinction of a reward-seeking behavior. Here, we used in vivo electrophysiology procedures in freely moving rats to investigate whether and how the BLA encodes the extinction of responding for sucrose. We recorded 330 neurons from 15 rats during a within-session extinction procedure following training under a partial reinforcement schedule. Several distinct populations of neurons change their response profiles as the rat ceases to respond for the omitted reinforcer. One population of neurons (32 of 330; 10%), which responded selectively to port entries in the presence, but not the absence, of sucrose during maintenance, subsequently developed a phasic response to port entries in the absence of sucrose during the extinction epoch only. The relative proportion of these reinforcement-omission neurons per rat was correlated with response intensity during extinction, as well as with the rate at which reward-seeking behavior was extinguished. A subpopulation of neurons responded with opposite phasic changes in activity to port entries in the presence of sucrose and to port entries during extinction, demonstrating that BLA neurons may contribute to the detection of value differences between expected and actual outcomes. Another population of neurons (47 of 330; 14%) responded to the empty port only during extinction. Because BLA neural correlates reflect the omission of an expected reward, these neuronal populations may contribute to the expression of behavior during extinction.