Role of amygdala central nucleus in feature negative discriminations.

Considerable behavioral evidence indicates that the disconfirmation of learned expectancies (“surprise”) can alter processing of stimuli present near the time of that surprise. Pearce and Hall (1980) proposed a model that related the associability of conditioned stimuli (CSs), their ability to participate in the formation of associations, to surprise. Within that model, the associability of a CS is proportional to the absolute value of the difference between the expected and actual value of the reinforcer on recent episodes that included that CS. Evidence suggests that such enhancements in CS associability that occur when reinforcers are unexpectedly omitted depend on the integrity of a neural system that includes the amygdala central nucleus (CeA) and its interactions with dopaminergic neurons of the substantia nigra pars compacta (SNc), cholinergic neurons of the substantia innominata (SI), and those latter neurons’ projections to posterior parietal cortex (PPC). Several behavioral phenomena attributed to these enhancements, including performance in a serial prediction task, unblocking with reinforcer downshifts, enhanced overshadowing after partial reinforcement, and augmented serial negative patterning learning, fail to occur in rats with disconnections among the elements of this system (see Holland & Maddux, 2010, for a review). Much of the evidence for these assertions come from experiments that used a serial prediction task first used by Wilson, Boumphrey, and Pearce (1992). In that task, rats received Pavlovian conditioning training in which the predictive validity of a visual CS was manipulated by altering its relation with an auditory CS. Rats in a “consistent” condition received training in which a light consistently predicted a tone throughout training, whereas rats in a “surprise” condition received training in which the validity of the light in predicting the tone was suddenly reduced from a consistent to a 50% relationship by omitting the tone on half of the trials. According to the Pearce-Hall (1980) model, this violation should cause an increase in the associability of the light. Indeed, subsequent light-food learning was more rapid in rats in the surprise condition (Wilson et al, 1992). However, rats with disruptions in function of CeA or SI (Chiba et al., 1995; Holland & Gallagher, 1993a, 2006), or functional disconnections between these 2 regions (Han et al., 1999), between CeA and SNc (Lee et al., 2006, 2008), or between SI and PPC (Bucci et al., 1998) all fail to display this enhanced associability after surprise. Similarly, rats with lesions of CeA (Holland & Gallagher, 1993b) or lesions that eliminate SI’s cholinergic innervation of PPC (Bucci et al., 1998) fail to show unblocking with reinforcer downshifts. Normally, prior training of a light-food relation “blocks” subsequent tone-food learning when a light + tone compound is paired with the same food reinforcer. However, under some circumstances, if the value of the reinforcer is reduced when the tone is added, tone-food learning is not blocked. This “unblocking” is especially likely when reinforcer value is lowered by omitting one of a series of reinforcer events (e.g., the second of two shocks or the second of two food deliveries; Dickinson, Hall, & Mackintosh, 1976; Holland, 1984, 1988). Within the Pearce-Hall model, this omission enhances the associability of the available cues, encouraging the association of the added tone with the remaining reinforcer. Because many learning theories (e.g., Rescorla & Wagner, 1972) predict that cues that accompany reductions in reinforcer value should acquire inhibitory learning, the observation of unblocking under these circumstances is an especially powerful confirmation of the importance of attentional processes specified by the Pearce-Hall (1980) model. Thus, observations that the same circuit-element disruptions that affect performance in the serial prediction task also affect unblocking when an expected reinforcer is omitted, support a role for this circuit in the enhancement of cue associability after the surprising omission of expected events. An anomaly within this framework is the lack of effects of CeA lesions on performance in the feature negative (FN) or conditioned inhibition (Rescorla, 1969) procedure (Holland, Thornton, & Ciali, 2000; Holland, Chik, & Zhang, 2001). In this procedure, a CS is reinforced when it is presented alone, but nonreinforced when it is accompanied by another, “feature” or “conditioned inhibitor” cue. As in the serial prediction task, this procedure involves partial reinforcement of a CS, and as in unblocking, it involves a reduction in the value of the reinforcer between presentations of a CS alone and those of a compound of that CS and another cue. Indeed, reduction of the value of the reinforcer to zero on compound trials in the FN procedure might be construed as the ultimate reduction in reinforcer value, and hence might also be expected to enhance or maintain the associability of both cues. In that case, rats with CeA lesions might be expected to exhibit slower learning than intact rats in this task, because they would not benefit from enhancements in cue associability normally produced by the surprising omission of the expected reinforcer. Nevertheless, Holland et al. (2000) found no effect of CeA lesions on the acquisition of performance in a serial FN procedure, in which an auditory cue was reinforced with food when it was presented alone, but nonreinforced when it was preceded by a light feature stimulus, and Holland et al. (2001) found no effects of CeA lesions on the acquisition of a simultaneous FN discrimination, in which an auditory cue was reinforced with food when it was presented alone, but not when it was presented simultaneously with a light cue. This latter observation was especially noteworthy because other rats in the same study demonstrated CeA lesion deficits in learning after the surprise treatment procedure in the serial prediction task. The present experiments were intended to further investigate the role of CeA in FN discriminations. In Experiments 1 and 2 we examined, in both sham- and CeA-lesioned rats, the acquisition of FN discriminations under training conditions that might be expected to influence the impact of surprise-induced associability enhancements. Regardless of those conditions, we found no effects of CeA lesions. In Experiment 3, we evaluated an alternative formulation of the Pearce-Hall (1980) model in which enhancement of the associability of the feature cue might not be anticipated in FN discrimination learning. Within that reformulation, the facilitatory effects of surprise on associability apply only to cues that generate the disconfirmed expectancy. This perspective corresponds to the casual view that attention is maintained to inconsistently treated cues (e.g., the target), but not to cues that consistently predict reinforcement or nonreinforcement (e.g., the feature). Accordingly, in Experiment 3 we directly compared the associability of feature and target cues after FN discrimination learning in CeA- and sham-lesioned rats.