Temporal encoding in trace conditioning

ROBERT P. COLE 0 1 ROBERT C. BARNET 0 1 RALPH R. MILLER 0 1 0 Copyright 1995 Psychonomic Society, Inc 1 State University ofNew York , Binghamton, New York Conditioned lick suppression in rats was used to explore the role of timing in trace conditioning. In Experiment 1, two groups of rats were exposed to pairings of a CS (CSl) with a US, under conditions in which the interstimulus interval (lSI) that separated CSI offset and US onset was either 0 or 5 sec. Two additional groups were also exposed to the same CSl~US pairings with either a 0 or a 5-sec lSI, and then received "backward" second-order conditioning in which CSI was immediately followed by a novel CS2 (i.e., CSl~CS2). A trace conditioning deficit was observed in that the CSI conditioned with the 5-sec gap supported less excitatory responding than the CSI conditioned with the O-secgap. However, CS2elicited more conditioned responding in the group trained with the 5-sec CSI-US gap than in the group trained with the O-sec CSI-US gap. Thus, the CSI-US interval had inverse effects on first- and second-order conditioned responding. Experiment 2 was conducted as a sensory preconditioning analogue to Experiment 1. In Experiment 2, rats received the CSI ~CS2 pairings prior to the CS1~US pairings (in which CS1 was again conditioned with either a 0 or a 5-sec lSI). Experiment 2 showed a dissociation between first- and second-order conditioned responding similar to that observed in Experiment 1. These outcomes are not compatible with the view that differences in responding to CSs conditioned with different ISIs are mediated exclusively by differences in associative value. The results are discussed in the framework of the temporal coding hypothesis, according to which temporal relationships between events are encoded in elementary associations. - In the typical Pavlovian conditioning procedure, an organism is exposed to pairings of a conditioned stimu lus (CS) and an unconditioned stimulus (US; Pavlov, 1927). One class of theorizing concerning classical con ditioning suggests that the organism forms an association between the CS and US representations that is based on these CS-US pairings. Once established, the CS-US as sociation ordinarily results in behavioral control by the CS when the CS is presented alone during a test. A fun damental theoretical question concerns how the infor mational content ofthese kinds ofassociations should be characterized (see Rescorla, 1988). Presumably, behav ioral control by a CS is observed because the CS informs the organism about an impending US. Indeed, some stu dents of learning have advanced the notion that these as sociations inform the organism not only that the US is going to occur, but also when in time the US will occur (e.g., Desmond & Moore, 1988; Logan, 1977; Matzel, Support for this research was provided by NIMH Grant 33881 and the SUNY-Binghamton Center for Cognitive and Psycholinguistic Sci ences. R.C.s. was supported by a Natural Sciences and Engineering Re search Council of Canada postgraduate scholarship. We thank Eric Lampinstein, Wendy Packer, and Danielle Scarinci for their assistance in data collection. We also thank Francisco 1. Esmoris-Arranz, Lisa M. Gunther, and Hua Yin for comments on earlier versions of the manu script. Finally, we gratefully acknowledge two anonymous reviewers for pointing out interpretive alternatives for Experiment I that led to the de sign ofExperiment 2. Requests for reprints should be addressed to R. R. Miller, Department of Psychology, SUNY-Binghamton, Binghamton, NY 13902-6000 (e-mail: ). -Accepted by previous editor, Vincent M. LoLordo Held, & Miller, 1988; Miller & Barnet, 1993; Schreurs & Westbrook, 1982). The idea that a memory may encode temporal attri butes of an experienced event is not new. In the study of human memory, for example, Tulving and Madigan (1970) suggested that memories of discrete events carry infor mation that reflects the points in time at which particular memories have been established. Memories may thus be temporally coded, which could provide organisms with the ability to make judgments about the temporal loca tions of other events. Jackson (1990; see also Green, 1989) has further suggested that humans may treat temporal re lationships between events as information. This informa tion could be stored in memory and, in turn, guide future behavior. These types of ideas concerning temporal information are captured in a recent view of Pavlovian conditioning which suggests that CS-US associations are composed of more than simple links between event representations. In this framework, the temporal relationships that exist among events during training are encoded as important attributes of the association. This view is called the tem poral coding hypothesis (Barnet, Arnold, & Miller, 1991; Matzel et al., 1988; Miller & Barnet, 1993). According to this hypothesis, close temporal contiguity between a CS and a US is sufficient for the formation of an association, but a predictive relationship between the CS and US is ordinarily necessary for the behavioral expression of that association. The assumption of the temporal coding hypothesis, that temporal contiguity is sufficient for associative learn ing, is challenged by the deficit in conditioned responding witnessed in simultaneous conditioning. If temporal contiguity is the primary variable that controls associa tive acquisition, one might expect that simultaneous con ditioning procedures would result in a stronger CS-US association than short-delay forward conditioning pro cedures, because simultaneous CS-US pairings are an example of perfect contiguity. Consequently,simultaneous CS-US pairings should produce more robust behavioral control by the CS than should short-delay forward CS-US pairings. However, research has repeatedly found that simultaneous conditioning is inferior to forward condi tioning (Heth & Rescorla, 1973; Pavlov, 1927; Smith, Coleman, & Gormezano, 1969; but see Mahoney & Ayres, 1976; Rescorla, 1980). Thus, it might be reasonable to assume that the simultaneous conditioning deficit does reflect a deficit in associative acquisition. In this view, simultaneous and forward conditioned associations dif fer in their associative strength. However, some authors (e.g., Barnet et aI., 1991; Matzel et aI., 1988) have main tained the position that contiguity is sufficient for asso ciative acquisition and suggest that deficient responding after simultaneous pairings reflects a performance fail ure rather than a learning failure. This failure in perfor mance may be due to the nature of the responses that experimenters typically assess. Most researchers have examined responses that are anticipatory in nature and thus serve as suitable tests for forward serial learning, but not necessarily so for simultaneous learning (see Barnet et aI., 1991, and Matzel et aI., 1988, for more de tailed discussions). A divergence in theorizing similar to that concerning sim (...truncated)