Consistent with previous reports using simple chain or concurrent schedules of reinforcement [e.g., 6
], BLA lesions did not impair learning or performance in concurrent chains schedules. The lesions in the current study did not affect rats’ sensitivity to primary reinforcement as indicated by their normal acquisition of preference (). All groups attained stable baseline preference in the concurrent chains schedule with VI 16-s initial links and FT 16-s terminal links in approximately 20 sessions. During these sessions, the groups did not differ in their preference for the initial link leading to the large reinforcer, suggesting that the BLA lesions did not disrupt sensitivity to differential reinforcer magnitude.
In contrast, pre-training BLA lesions disrupted nose poking during the terminal links. When a large reinforcer was to be delivered, nose poking remained highly accurate throughout the terminal link in all groups except PRE lesioned rats. The nose poking of PRE lesioned rats was similar during both large and small reinforcer terminal links, with accuracy declining over seconds (). Since tone frequency was the only stimulus distinguishing small and large reinforcer terminal links, these data suggest that pre-training BLA lesions impaired learning about the tone frequency-reinforcer magnitude relationship.
The BLA is well-known for its role in conditioned reinforcement, which relies on stimulus-reinforcer relationships [1
]. Impaired learning about conditioned reinforcers may not, however, be detected in the acquisition of preference in concurrent chains schedules. For example, although conditioned reinforcers (i.e., terminal link stimuli) contribute to initial link preference [38
], pigeons prefer an initial link leading to larger reinforcement even when the terminal links are not differentially signaled [39
]. In the current study, the location of the lever associated with large reinforcement was consistent during baseline sessions. Location may, therefore, have been a salient stimulus directing initial link choice. This could explain why BLA lesions, which are critical for conditioned reinforcement [1
], did not disrupt acquisition of preference in concurrent chains in this study.
Rats with pre-training BLA lesions were also insensitive to reversal of the reinforcer magnitudes during the first 16 trials of the session (). One possible explanation is that pre-training BLA lesions impaired learning about tone-reinforcer relationships in PRE lesioned rats, as suggested by terminal link nose poking. Such an impairment may have prevented them from discriminating changes in the tone-reinforcer relationship that could be a basis for adaptation of initial link choices in normal rats. For example, behavioral adaptation after reinforcer omission occurs, in part, because omission violates the animal’s expectation [40
]. A rat expecting, for example, to receive 150 µl sucrose after a 15 kHz tone would be more surprised to receive 50 µl sucrose after a 15 kHz tone during a reversal session compared to a rat that had not learned the tone-reinforcer relationships. With greater surprise, behavior would be expected to change more rapidly [41
], a principle that also applies to instrumental conditioning [42
]. The PRE lesioned rats changed their preference to some extent during the last 16 trials, indicating that they were not completely insensitive to the reinforcer magnitude reversal.
In a conditional discrimination protocol, BLA lesions disrupt rats’ reversal of responding when switching from familiar to new contingencies [43
]. The current protocol differs from conditional discrimination protocols. Whereas the initial link response scheduled for reinforcement was not signaled, the terminal link stimuli signaled the magnitude and location of reinforcement, although not a response contingency. Sucrose was always delivered at the end of the terminal link, but a nose poke was necessary for consumption. Both reversal of responding in a conditional discrimination and adaptation of preference to reinforcer magnitude reversal may involve learning about stimulus-reinforcer relationships, a process supported by the BLA [1
]. Studies using other protocols suggest that the amygdala is important for behavioral control by differential reinforcer magnitudes, e.g., delayed responding to stimuli predicting relatively large reinforcers [44
], memory for reinforcer magnitude changes [45
], and for acquisition of a conditional discrimination in which the discriminative stimuli are different concentrations of sucrose solution [46
]. Consistent with these results, the nose poke accuracy of PRE rats with BLA lesions decreased across both large and small reinforcer terminal links in the current study (), whereas other groups maintained accuracy throughout the large reinforcer terminal links. PRE rats with BLA lesions were, however, sensitive to the differential reinforcer magnitudes as indicated by normal preference for the initial link associated with large, delayed reinforcement over the initial link associated with small, delayed reinforcement. Pre-training BLA lesions may have disrupted rats learning about the sensory, but not the reinforcing, properties of the differential reinforcer magnitudes.
The PRE and POST groups differed in the total number of training sessions and in the number of days between surgery and the reinforcer magnitude reversals (). POST rats experienced approximately 9 additional training sessions because they were re-trained to stable baseline performance after surgery. Overtraining can render behavior resistant to changes in reinforcement [47
]. Indeed, when the reinforcer magnitudes were reversed, POST rats changed their preference less than PRE rats as the trials progressed (), which could result from additional training. On the other hand, POST rats were slightly, but significantly, less accurate than PRE rats during small reinforcer terminal links, but one would expect greater accuracy with more training sessions. It is unlikely that 9 additional training sessions can account for the differences between the PRE and POST lesioned rats in response to the reinforcer magnitude reversal. In addition, the PRE groups experienced more days between surgery and the reinforcer magnitude reversals compared to POST groups. Typically, however, functional recovery increases with time after neural damage [e.g., 48
]. Despite an approximately three-fold greater lesion-to-test interval in PRE lesioned rats (~45 days) compared to POST lesioned rats (~15 days), PRE lesioned rats showed significant behavioral impairment. Furthermore, these impairments depended on the magnitude of neural damage. Partially lesioned rats performed similarly to intact rats. The data are unlikely, therefore, to be explained solely by differences in the lesion-to-test interval between PRE and POST groups.
The effect of reversing the reinforcer magnitudes on initial link preference carried over into the subsequent session when the original contingencies were reinstated. Baseline preference for the large reinforcer initial link was lower in the session after the reversal compared to the session before the reversal for all groups. This suggests that the BLA does not contribute to rats’ estimation of past reinforcement used to determine current preference.
Researchers have assumed that studies of choice in transition will provide information about both the processes supporting preference acquisition and animals’ matching of response allocation to reinforcers between concurrent schedules of reinforcement [e.g., 25
]. With respect to the former, these data show that pre-training BLA lesions do not affect preference acquisition, but do disrupt rats’ immediate changes in choice behavior after reversal of the reinforcer magnitudes. The lesions did not disrupt the effect of past reinforcement contingencies on current choice. This suggests that distinct processes underlie preference acquisition, the influence of past reinforcement contingencies on current preference, and the adaptation of preference to local changes in reinforcement contingencies. BLA activity appears to support the latter, perhaps by allowing animals to learn about various attributes of reinforcers [50
] that provide a basis for rapid discrimination of changes. Future studies could evaluate the role of the BLA in behavioral adaptation when other properties of the primary reinforcer or the conditioned reinforcer (terminal link stimulus) are manipulated.