Role of amygdala central nucleus in feature negative discriminations

Abstract

Consistent with a popular theory of associative learning, the Pearce-Hall (1980) model, the surprising omission of expected events enhances cue associability (the ease with which a cue may enter into new associations), across a wide variety of behavioral training procedures. Furthermore, previous experiments from this laboratory showed that these enhancements are absent in rats with impaired function of the amygdala central nucleus (CeA). A notable exception to these assertions is found in feature negative (FN) discrimination learning, in which a "target" stimulus is reinforced when it is presented alone but nonreinforced when it is presented in compound with another, "feature" stimulus. According to the Pearce-Hall model, reinforcer omission on compound trials should enhance the associability of the feature relative to control training conditions. However, prior experiments have shown no evidence that CeA lesions affect FN discrimination learning. Here we explored this apparent contradiction by evaluating the hypothesis that the surprising omission of an event confers enhanced associability on a cue only if that cue itself generates the disconfirmed prediction. Thus, in a FN discrimination, the surprising omission of the reinforcer on compound trials would enhance the associability of the target stimulus but not that of the feature. Our data confirmed this hypothesis and showed this enhancement to depend on intact CeA function, as in other procedures. The results are consistent with modern reformulations of both cue and reward processing theories that assign roles for both individual and aggregate error terms in associative learning.

Figure 1

Photomicrographs of typical sham (A) and neurotoxic (B) lesions of the amygdala central nucleus (CeA). BLA refers to the basolateral amygdala; IC to the intercalated nuclei.

Figure 2

Results of Experiment 1. As in previous studies, rats with CeA lesions showed deficits in the acquisition of conditioned orienting responses (activity; Panel A) but not conditioned food-related responses (food cup; Panel B) to the reinforced noise (N+) conditioned stimulus (CS) during the initial acquisition phase of Experiment 1. Most important, discrimination of food cup responding between reinforced noise (N+) and nonreinforced light + noise (LN−) compound trials in feature negative discrimination training was unaffected by the lesions (Panel C). The abscissa points labeled “pre” refer to responding in the periods immediately prior to CS presentations. The designations CeA and sham refer to rats with neurotoxic or sham lesions of the amygdala central nucleus (CeA), respectively.

Figure 3

Results of Experiment 2. Neither food cup responding to the reinforced light conditioned stimulus (CS) during the initial acquisition phase (Panel A) nor feature negative discrimination learning (Panel B) was affected by CeA lesions. L+ refers to responding during the reinforced light and NL− refers to responding during the nonreinforced noise + light compound. The abscissa points labeled “pre” refer to responding in the periods immediately prior to CS presentations. The designations CeA and sham refer to rats with neurotoxic or sham lesions of the amygdala central nucleus (CeA), respectively.

Figure 4

CeA lesions had no effects on conditioned food cup responding in either the initial acquisition (Panel A) or discrimination training (Panel B) phases of Experiment 3. CS+ and CS− refer to reinforced and nonreinforced conditioned stimuli. Rats in Groups F and TA received feature negative discrimination training, whereas rats in Groups C and TC received simple discrimination training (see text and Table 1 for more details). The designations CeA and sham refer to rats with neurotoxic or sham lesions of the amygdala central nucleus (CeA), respectively.

Figure 5

CeA lesions had no effects on the acquisition of food cup responding during the compound conditioning (overshadowing) phase of Experiment 3. In separate groups of rats, a novel light was compounded with either the feature (F) or target (TA) stimulus from a feature negative discrimination, or a consistently reinforced (TC) or nonreinforced (C) stimulus from the control discrimination, and paired with the delivery of a large magnitude high concentration sucrose reinforcer (see text and Table 1 for more details.) The designations CeA and sham refer to rats with neurotoxic or sham lesions of the amygdala central nucleus (CeA), respectively.

Figure 6

Results of the test session of Experiment 3. (Panel A) Responding to the light stimulus that was first introduced in the prior compound conditioning (overshadowing) phase. Lower levels of responding to the light indicate greater overshadowing by the cue that accompanied it in compound conditioning. CeA lesions interfered with the ability of the target of a feature-negative discrimination (Group TA) to overshadow conditioning to that light, but not with the ability of a consistently-reinforced stimulus to do so (Group TC). (Panel B) Responding to the auditory stimulus that accompanied the light stimulus during compound conditioning. In both panels, group designations indicate the nature of training to the auditory cue used in the overshadowing phase. CeA lesions interfered with the ability of a target of a feature-negative discrimination (Group TA) to acquire additional conditioned responding in that phase. TA and F refer to the target and feature from a feature negative discrimination, respectively, and TC and C refer to the consistently reinforced and nonreinforced stimuli (respectively) from a simple discrimination. The designations CeA and sham refer to rats with neurotoxic or sham lesions of the amygdala central nucleus (CeA), respectively.