Formation of excitatory and inhibitory associations between absent events.

Most learning theorists agree that through associative learning, conditioned stimuli (CSs) can come to activate representations of their unconditioned stimulus (US) referents. These associatively-activated event representations may serve many functions, including mediating the performance of conditioned responses (CRs) (Rescorla, 1973), interacting with real events in overshadowing and potentiation (Holland, 1983), and participating in new learning about represented, but physically absent events (Holland, 1981). The experiments reported here examined the nature of tone-sucrose learning produced when associatively-activated representations of those events were paired in the absence of either of the events themselves. Holland (1981) found that rats could acquire a food aversion when an associatively-activated representation of food was paired with toxin-induced illness. In one experiment, rats first received pairings of one auditory CS with wintergreen-flavored sucrose and another CS with peppermint-flavored sucrose. Then, the rats were given injections of lithium chloride (LiCl) after presentations of one of those CSs in the absence of either sucrose reinforcer. In a subsequent test, the rats consumed less of the flavored sucrose whose CS partner had been paired with LiCl. However, there was no evidence for a direct CS-LiCl association. Holland (1981) concluded that excitatory flavor-illness associations could be established when an associatively-activated (imaginary) representation of the flavor was paired with the actual induction of illness. Similarly, Holland and Forbes (1982) found that extinction of a previously-established food aversion could be facilitated if an associatively-activated representation of that food was presented repeatedly in the absence of illness. In one experiment, two auditory CSs were first paired with two flavored sucrose reinforcers, as in Holland’s (1981) study. Then, aversions were established to both flavored reinforcers by pairing each of them directly with LiCl. Next, the rats were given repeated presentations of one of the auditory CSs alone. Finally, all rats received test presentations of each of the two flavors. Although initially consumption of both flavors was suppressed, over the course of continued testing, all rats consumed more of the flavor whose CS partner had been presented in extinction. Thus, the flavor representation activated by the CS alone substituted for the flavor itself in extinction learning. Many current theories of extinction posit that it involves the acquisition of inhibitory associations between the extinguished cue and the reinforcer with which it was originally paired. The implication of this position for Holland and Forbes’s (1982) results is that inhibitory flavor-illness associations were formed when associatively-activated representations of both flavor and illness were paired. To accommodate Holland’s (1981) and Holland and Forbes’s (1982) results within contemporary learning theory, Holland (1983) suggested modifications of Wagner’s (1981) SOP model of learning. In that model, memory representations (nodes) may be in any of three activity states, A1, A2 or I. An event enters the focal A1 state only by direct activation by the physical event itself. By contrast, an event enters the more marginal A2 state either by spontaneous decay from the A1 state or by retrieval by an A1- or A2-state node that is associated with that event. Finally, events enter the inactive, resting I state by spontaneous decay from the A2 state. Within this model, excitatory associations between a CS and US are formed when their representations are processed simultaneously in the A1 state, and inhibitory CS-US associations are formed when the CS node is in the A1 state and US node is in the A2 state. Thus, excitatory associations are formed between CS and US only when they are both physically presented, whereas inhibitory associations are formed when the CS is physically presented together with an associatively-activated representation of the US. SOP made no provision for learning when the CS representation is in the A2 state, rather than in the A1 state, and thus could not readily account for either mediated learning or mediated extinction. Holland (1983) suggested that representations in the A2 state, such as associatively-activated representations, could also enter into associations as CSs, albeit with a lower probability than A1-state (directly-presented) CSs. Thus, consistent with his mediated learning and extinction results, Holland (1983) suggested that “A2-Al” learning (in which the CS and US are in the A2 and A1 states, respectively) would be excitatory and “A2-A2” learning would be inhibitory. In keeping with the original SOP model, the establishment of excitatory or inhibitory associations with the US would be determined by the status of the US node (A1-state or A2-state, respectively), regardless of whether the CS representation was directly- or associatively activated. Thus, both A1-A1and A2-A1 learning would be excitatory and both A1-A2 and A2-A2 learning would be inhibitory. However, Dwyer and his colleagues have amassed considerable evidence that the pairing of two associatively-activated event representations produces excitatory associations between those events (Dwyer, 1999, 2000, 2001, 2003; Dwyer, Mackintosh, & Boakes, 1998), rather than the inhibitory A2-A2 learning Holland (1983) might have anticipated. For example, in one experiment, Dwyer et al. (1998) first gave rats access to a peppermint solution in context one and to an almond + sucrose solution in context two. Next, almond alone was administered in context one in one group of rats and in context two for another group. A final consumption test revealed a greater preference for peppermint in the rats that received almond-alone in context one. Dwyer et al. (1998) asserted that this preference reflected the establishment of A2-A2 peppermint-sucrose associations: in those rats the associative activation of the peppermint flavor by context one cues was accompanied by the associative activation of sucrose by almond. By contrast, the rats in the other group had no opportunity for peppermint-sucrose learning because context two would not have activated a representation of peppermint. Dwyer et al. (1998) interpreted their results within another modification of SOP, offered by Dickinson and Burke (1996), which was originally intended to deal with observations of retrospective revaluation in studies of human causality judgments. Within this framework, excitatory associations are formed between two nodes when they are both activated in the same state (i.e., A1-A1 or A2-A2) and inhibitory associations are formed when the two nodes are activated in different states (i.e., A1-A2 and A2-A1). Clearly, for more thorough understanding of the rules of association, Dwyer’s observation of excitatory A2-A2 learning and Holland’s observation of inhibitory A2-A2 learning need to be reconciled. A simple assumption motivating the present experiments was that A2-A2 learning might be either excitatory or inhibitory, depending on the nature of relations arranged between them, especially temporal relations. Indeed, Dwyer (2003) noted the potential importance of temporal contiguity in determining the outcome of mediated learning experiments. However, the use of unspecified contextual cues and agents that induce illness with delayed, gradual onsets makes an analysis of the role of temporal factors difficult. Recently, Wheeler, Sherwood, and Holland (2008) investigated the nature of A2-A2 learning between two auditory stimuli when visual associates of those stimuli were paired. Using designs based on sensory preconditioning procedures, Wheeler et al. (2008) found evidence for both excitatory and inhibitory learning between associatively-activated event representations, depending on the temporal arrangement of cues. They first administered light1→ noise and light2→ tone pairings, followed by light1-light2 compound presentations, designed to establish A2-A2 associations between noise and tone. The presence of those associations was evaluated by first pairing the tone with sucrose and then testing responding to the noise. Wheeler et al. (2008) found evidence for excitatory noise-tone associations when the elements of the compound were administered in the order light1→ light2, but inhibitory associations when the elements were presented simultaneously or in the opposite order (light2→ light1). Wheeler et al. (2008) concluded that the nature of A2-A2 learning is neither always excitatory nor always inhibitory, but rather depends on task parameters, such as the temporal arrangement of stimuli. Miller and Matute (1996) noted that the results of conditioning experiments may often depend on the biological significance of the events involved. It is possible that Wheeler et al.’s (2008) observations depended on their use of relatively neutral A2-state events. In the present experiments, we extended Wheeler et al.’s (2008) findings by examining the nature of tone-sucrose learning when associatively-activated representations of those events were presented jointly. In Experiment 1 we found evidence for strong excitatory A2-A2 learning, in Experiment 2 we evaluated alternative accounts for those results, and in Experiment 3 we examined the effects of variation in the temporal arrangement of the two associatively-activated event representations on the nature of learning obtained.