The effects of basolateral amygdala lesions on unblocking

Most theories of associative learning assert that violation of learned expectancies can produce alterations in processing of the cues or reinforcers present near the time of those surprising outcomes. A common arena for evaluating those theories is the blocking/unblocking paradigm. In blocking, prior conditioning of one cue is found to interfere with learning about a second cue if a compound of those two cues is subsequently paired with the same reinforcer. Because that reinforcer is already well-predicted by the first cue when the new cue is introduced, processing of the reinforcer itself (e.g., Rescorla & Wagner, 1972; Sutton & Barto,1981) or the added cue (e.g., Esber & Haselgrove, 2011; LePelley, 2004; Mackintosh, 1975; Pearce & Hall, 1980; Pearce & Mackintosh, 2010) is minimized, and so the association between that cue and the reinforcer is not learned. However, if the value of the reinforcer is altered when the new cue is added, such learning is once again evident. This observation, termed unblocking, has been observed with both increases (“upshifts”; Kamin, 1968; Holland, 1984, 1988) and decreases (“downshifts”; Dickinson & Mackintosh, 1976; Holland, 1984; 1988). Much attention has been focused on the downshift case, because reinforcer and cue processing theories make opposite predictions. When reinforcer value is decreased, the reward prediction error is negative, and reinforcer-processing theories such as the Rescorla-Wagner (1972) model predict that the added cue will acquire inhibitory learning. By contrast, cue-processing models such as the Pearce-Hall (1980) model predict that excitatory learning will accrue to the added cue, because changes in cue effectiveness (“associability”) are assumed to be driven by an unsigned error term. Thus, within these later theories, any surprising outcome, yielding either positive or negative prediction error, could enhance or restore the associability of the added cue, enabling its association with the reinforcer presented on compound trials. Research from our laboratory, using a number of experimental paradigms (Holland & Maddux, 2010) identified components of brain circuitry critical to the enhancement of cue associability after negative prediction error consequent to the omission of expected events, including the amygdala central nucleus (CeA), the substantia nigra pars compacta, the sublenticular substantia innominata, and the posterior parietal cortex. Investigations of unblocking with a downshift found that rats with lesions of CeA failed to show normal excitatory learning about the added cue (Holland & Gallagher, 1993b; Holland & Kenmuir, 2005), but were intact in their learning of inhibitory associations between the added cue and the omitted reinforcer (Holland & Kenmuir, 2005). By contrast, CeA lesions had no effect on additional learning that accrued when reinforcer value was increased in an unblocking design (Holland & Gallagher, 1993b), even when steps were taken to insure that the unblocking obtained reflected enhanced cue associability rather than enhanced processing of the unexpected new reinforcer (Holland, 2006). Results such as these led us to conclude that the role of CeA in associability enhancements was limited to cases involving negative prediction errors (Holland & Maddux, 2010). Notably, these observations are consistent with the results of a recent electrophysiological study in which we observed CeA neurons that responded to downshifts in reward value, but did not find significant numbers of neurons that responded to upshifts (Calu et al., 2010). However, considerable evidence indicates that another amygdala subregion, the basolateral amygdale (BLA, comprising the lateral, basal, basolateral, basomedial, and accessory basal nuclei) encodes reinforcer value (e.g. Holland & Gallagher, 2004). Furthermore, a study that used methods similar to those of Calu et al. (2010) found a significant number of BLA neurons that responded to both decreases and increases in US value (Roesch et al., 2010). Thus, these neurons provided precisely the unsigned error signal specified by theories such as the Pearce-Hall (1980) model. From these observations it seems reasonable to suggest that the BLA might be critical to processing of unsigned reinforcer prediction error signals that enhance cue associability in unblocking. The experiments reported here considered whether enhanced learning with upshifts in reinforcer value might be mediated by the BLA. In Experiment 1, following the experimental procedures used by Holland and Gallagher (1993b), we found no evidence for a BLA role in unblocking with upshifts in reinforcer value. However, because upshift unblocking could in principle result solely from the greater effectiveness of the reinforcer when its value was increased (as expected within theories like the Rescorla-Wagner model, 1972), it could be argued that this study did not provide a fair test of BLA’s involvement in the enhancement of cue associability after upshifts in reward value, as predicted by theories such as the Pearce-Hall (1980) model. Therefore, in Experiment 2, we examined the effects of BLA lesions on upshift unblocking in a more complex paradigm used previously to disentangle cue- and reinforcer-processing contributions to upshift unblocking (Holland, 1988, 2006).